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Veronica: Iridoids and cornoside as chemosystematic markers Article in Biochemical Systematics and Ecology · October 2005 DOI: 10.1016/j.bse.2005.03.001
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Biochemical Systematics and Ecology 33 (2005) 1031e1047 www.elsevier.com/locate/biochemsyseco
Veronica: Iridoids and cornoside as chemosystematic markers Søren Rosendal Jensen a,*, Dirk C. Albach b,1, Takao Ohno c, Rene´e J. Grayer d a
Department of Chemistry, The Technical University of Denmark, DK-2800 Lyngby, Denmark b Department of Systematic and Evolutionary Botany, Institute of Botany, University of Vienna, Rennweg 14, A-1030 Vienna, Austria c Center for Instrument Analysis, Niigata University, 950-2181, Ikarashi-2, 8050 Niigata, Japan d Royal Botanic Gardens, Kew, Richmond, Surrey TW9 3AB, UK Received 15 October 2004; accepted 10 March 2005
Abstract The iridoid glucoside, ajugol, and the phenylethanoid glucoside, cornoside, have been isolated from species of Veronica (Plantaginaceae) for the first time. The presence of these compounds has been screened in 18 plant accessions belonging to 15 species of Veronica (Plantaginaceae), by isolation or NMR spectroscopy of crude extracts. In addition, the distribution of iridoids in the genus has been reviewed, using mainly the published data of isolated compounds. Using the recent expansion and reclassification of the genus based on DNA-sequence results as the model, we find that the genus is rather homogeneous with regard to the distribution of iridoid glucosides, aucubin and/or catalpol as well as 6-O-esters of catalpol being universally present in 10 of the 12 subgenera for which data exist. Only the two subgenera Pocilla and Chamaedrys deviate from this pattern. Pocilla is heterogeneous; in this subgenus, species in subsect. Agrestes contain the standard iridoid garniture, while species in subsect. Biloba do not contain the 6-O-esters of catalpol, but ajugol instead. Veronica intercedens (subsect. Subracemosae) differs from the remainder of the subgenus in only
* Corresponding author. Tel.: C45 45252103; fax: C45 45933968. E-mail address:
[email protected] (S.R. Jensen). 1 Present address: Instiut fu¨r Spezielle Botanik, Johannes Gutenberg-Universita¨t Mainz Bentzelweg 9b, D-55099 Mainz, Germany. 0305-1978/$ - see front matter Ó 2005 Elsevier Ltd. All rights reserved. doi:10.1016/j.bse.2005.03.001
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containing 5-hydroxylated iridoids (melittoside and globularifolin) and is so far the only species within the genus in which such compounds have been detected. These chemical differences are clearly reflected in the DNA-based phylogram of the subgenus. Subg. Chamaedrys appears homogeneous in lacking iridoids or only containing these in small amounts, but instead half of the investigated species contained the phenylethanoid glucoside cornoside. The distribution of this compound in angiosperms is reviewed; cornoside often substitutes iridoid glucosides in plants where these are expected to be present. The chemical results of Veronica fit in very well with the phylogenetic implications of the DNA-sequence results. Ó 2005 Elsevier Ltd. All rights reserved. Keywords: Veronica; Veroniceae; Plantaginaceae; Chemotaxonomy; Iridoid glucosides; Ajugol; Cornoside; Phenylethanoid glycosides; Phylogeny; DNA sequencing
1. Introduction Recently it has been shown, using DNA-sequence analysis, that the circumscription and classification of the genus Veronica should be completely revised (Albach and Chase, 2001; Albach et al., 2004a,b) and a new classification has been proposed in which Veronica is divided into 13 subgenera (Albach et al., 2004c; Table 1). This classification differs considerably from previous classifications, which were mainly based on morphology. Therefore, it would be interesting to investigate whether characters from disciplines other than morphology would support the new arrangements of the species based on DNA-sequence results. In turn, dendrograms based on molecular data can be used to assess the usefulness of characters from other areas of research. One branch of plant science that has greatly benefited from the comparison with DNA-sequence analyses is chemotaxonomy (Grayer et al., 1999; Jensen, 2000; Jensen et al., 2002). Therefore, one of the objectives of the present paper is to show that chemotaxonomic characters are useful to support relationships retrieved in DNA-sequence analyses. The distribution of iridoids in the genus Veronica has been intensively investigated by Grayer-Barkmeijer (1973, 1979) and Taskova et al. (2002). In these papers, taxonomic analyses of the distribution of compounds in the genus were performed in the light of classifications that pre-dated molecular systematic analyses, but recently Taskova et al. (2004) made a comparison between the new classification of Veronica based on molecular analyses and the distribution of iridoids in the genus. However, these investigations were primarily performed using chromatographic methods which have proved very useful, but misidentifications can easily occur, e.g. when unknown compounds give similar Rf values and colour reactions as the known standards. Therefore, a safer approach is to isolate the compounds from the plants and identify them by NMR spectroscopy. In recent years, many species of Veronica have been investigated in this way, and we therefore decided to review the occurrence of iridoids in the genus by using data from the literature for plants from which the iridoids have actually been isolated and identified. In the course of this work, we also investigated 15 additional species, some
Table 1 Taxonomic history of taxa mentioned in the text Bentham (1846)
von Wettstein (1891)
Stroh (1942)
Elenevsky (1977)
Subg. Veronica (V. alpina, V. bellidioides) Subg. Veronica (V. officinalis)
Sect. Veronicastrum, subsect. Alpinae Sect. Chamaedrys, subsect. Strictiflorae Sect. Beccabunga
Sect. Veronicastrum, subsect. Alpinae Sect. Chamaedrys, subsect. Strictiflorae Sect. Beccabunga
Sect. Veronicastrum, subsect. Alpinae Sect. Chamaedrys, subsect. Officinalis Sect. Beccabunga
Sect. Veronicastrum, subsect. Alpinae Sect. Veronica, subsect. Veronica Sect. Beccabunga
Sect. Pseudolysimachia
Sect. Pseudolysimachia
Synthyris
Sect. Pseudolysimachia Synthyris
e
Sect. Pseudolysimachium e
Sect. Omphalospora, subsect. Subracemosae
Sect. Omphalospora, subsect. Cymbalariae
Sect. Alsinebe, subsect. Megasperma
Sect. Diplophyllum, subsect. Cymbalariae
Sect. Omphalospora, subsect. Subracemosae
Sect. Omphalospora, subsect. Subracemosae Sect. Veronicastrum, subsect. Fruticulosae e
Sect. Alsinebe, subsect. Pellidosperma
Sect. Alsinebe, subsect. Pellidosperma
Sect. Veronicastrum, subsect. Diffusae Sect. Beccabunga
e
Sect. Alsinebe, subsect. Microsperma Sect. Alsinebe, subsect. Agrestis
Sect. Veronicastrum, subsect. Saturejoides Sect. Stenocarpon, subsect. Stenocarpon Sect. Digitatae
Subg. Beccabunga (V. anagallis-aquatica, V. undulata) Subg. Pseudolysimachium (all spp.) Subg. Synthyris (V. besseya, V. plantaginea) Subg. Cochlidiosperma (V. hederifolia, V. cymbalaria) Subg. Pellidosperma (V. triphyllos) Subg. Stenocarpon (V. kellererii) Subg. Stenocarpon (V. ciliata) Subg. Triangulicapsula Subg. Pocilla, subsection Pocilla* Subg. Pocilla, subsection Biloba
e Sect. Beccabunga Sect. Veronicastrum, subsect. Annuae Sect. Veronicastrum, subsect. Annuae and Sect. Omphalospora, subsect. Agrestes Sect. Omphalospora, subsect. Subracemosae
Sect. Omphalospora, subsect. Agrestes
Sect. Alsinebe, subsect. Biloba
Sect. Alsinebe, subsect. Biloba (continued on next page)
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Sect. Omphalospora, subsect. Subracemosae
Sect. Alsinoides
S.R. Jensen et al. / Biochemical Systematics and Ecology 33 (2005) 1031e1047
Taxa according to Albach et al. (2004c), used in this paper
von Wettstein (1891)
Stroh (1942)
Elenevsky (1977)
Subg. Pocilla, subsection Subracemosae
Sect. Omphalospora, subsect. Subracemosae
e
Subg. Pentasepalae (V. fuhsii, V. liwanensis, V. multifida, V. orientalis, V. pectinata, V. thymoides) Subg. Chamaedrys (V. verna, V. arvensis, V. dillenii) Subg. Chamaedrys (V. chamaedryoides, V. chamaedrys, V. laxa, V. magna, V. micans, V. micrantha, V. orbelica, V. vindobonensis) Subg. Hebe
Sect. Chamaedrys, mult. subsect.
Sect. Chamaedrys, subsect. Pentasepalae
Sect. Alsinebe, subsect. Acinifolia p.p. and subsect. Alsinebe p.p. Sect. Chamaedrys, mult. subsect.
Sect. Alsinebe, subsect. Cardiocarpae and subsect. Brevistylae Sect. Veronica, mult. subsect.
Sect. Veronicastrum, subsect. Annuae Sect. Chamaedrys, subsect. Multiflorae
e
Sect. Alsinebe, subsect. Microsperma Sect. Chamaedrys, subsect. Euchamaedrys
Sect. Alsinebe, subsect. Alsinebe Sect. Veronica, subsect. Multiflorae
Sect. Hebe, three subsects.
e
e
Subg. Derwentia
Sect. Chamaedrys, subsect. Calycina and Sect. Hebe, subsect. Labiatae
Sect. Hebe and Sect. Pygmaea Sect. Chamaedrys, subsect. Calycina and Sect. Labiatoides
Sect. Chamaedrys, subsect. Calycina and Sect. Labiatoides
Sect. Veronica, subsect. Calycina and Sect. Labiatoides
Sect. Chamaedrys, subsect. Multiflorae
* Subsection Pocilla (Dumort.) Albach comb. nov., rather than subsection Agrestes Benth., is the taxonomically correct name because it includes the type of subgenus Pocilla (Dumort.) M. M. Mart. Ort., Albach and M. A. Fisch. and section Pocilla Dumort. Fl. Belg.: 35 1827 [basionym], V. agrestis.
S.R. Jensen et al. / Biochemical Systematics and Ecology 33 (2005) 1031e1047
Bentham (1846)
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Table 1 (continued ) Taxa according to Albach et al. (2004c), used in this paper
S.R. Jensen et al. / Biochemical Systematics and Ecology 33 (2005) 1031e1047
1035
of which were studied by analyses of the NMR spectra of the crude extracts, a method more reliable than chromatography. We discuss the distribution of iridoid glycosides in the light of the new classification derived from the DNA-sequence results.
2. Materials and methods 2.1. General procedures 1
H and 13C NMR spectra were recorded on a Varian Mercury-300 MHz or a Varian Unity plus 500 MHz instrument in D2O or CD3OD using the solvent peak as the internal standard. The isolated compounds were identified by their 1H and 13C NMR spectra by comparison with spectra of known standards. In the cases where only small herbarium samples were available, individual glycosides were solely identified by their characteristic signals: cornoside (2; d 2.1, 4.3, 6.2 and 7.1); cornoside aglucone (d 2.1, 6.2 and 7.1); rengyolone (d 6.0 and 6.9); verbascoside (4; d 1.0, 2.7, 6.2 and 7.5); aucubin (5; d 4.5, 5.8 and 6.2). The amount of mannitol (1) in the carbohydrate fraction was based on the relative intensity of the three peaks (d 64.6, 70.7 and 72.2) (Bock and Pedersen, 1983) in the 13C NMR spectrum (D2O) when compared to other sugar signals in the sample. 2.2. Plant sampling In the course of this study, we have focused on subgenus Chamaedrys to determine whether cornoside could also be a chemotaxonomic marker. Voucher specimens for the plants used in this study are listed in Table 2. We here use the combination Veronica micans in place of V. chamaedrys subsp. micans for the ease of discussion, although the combination has not been validly published. 2.3. Work-up of plant material 2.3.1. Herbarium samples Dry plant material (35e80 mg of aerial parts) of species from subgenus Chamaedrys (Table 2) was extracted separately by blending in EtOH (50 ml). The mixture was brought to the boiling point and then left to stand at room temperature for 3 days. After filtering, each extract was evaporated and partitioned in H2O:Et2O (25 ml each); the aqueous layer was concentrated to give the crude extract. The content of glycosides was analyzed by inspection of the 1H NMR spectra in D2O. 2.3.2. Larger samples See individual plants for work-up details (Table 3). These extracts were processed by preparative chromatography using a Merck Lobar RP-18 column size B. The initial eluent was H2O followed by H2O:MeOH mixtures (15:1 to 4:5) and finally by MeOH. The isolated compounds were identified by means of 1H NMR spectroscopy.
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Table 2 Voucher specimens for the species investigated in the present work Species
Voucher
Origin e collection year
V. arvensis
IOK-2/2004, WU Takao Ohno #1, WU Albach 393, WU IOK-3/1999, WU Schneeweiss 24.4.1995, WU Handel-Mazetti 26.6.1917, WU Albach and Schneeweiss Ge00/186, WU M. A. Fischer 4-7-1971, WU Martı´ nez-Ortega 135, SALA Martı´ nez-Ortega MO1754, SALA Albach 514, WU Greimler 14.5.1995, WU Albach 283, WU IOK-3/2003, WU
Denmark e 2004 Japan e 2004 Greece e 2001 Denmark e 1999 Austria e 1995 China e 1917 Georgia e 2000
V. V. V. V. V.
chamaedryoides chamaedrys dillenii laxa magna
V. micans V. micrantha V. V. V. V.
orbelica verna vindobonensis argute-serrata
IOK-4/2003, WU (Albach 685, WU) V. biloba
IOK-5/2003, WU
V. campylopoda
IOK-6/2003, WU
V. longifolia
IOK-10/2003, WU
Austria e 1971 Iberian Peninsula e 1996 Iberian Peninsula e 2004 Bulgaria e 2001 Austria e 1995 Austria e 2000 cultivated in Denmark e 2003 seed origin: near Catak, Turkey Cultivated in Denmark e 2003 seed origin: Murat valley near Tutak, Turkey cultivated in Denmark e 2003 seed origin: near Catak, Turkey cultivated in Denmark e 2003 seed origin: near Catak, Turkey cultivated in The Botanical Garden, Copenhagen
3. Results and discussion The results of the present investigations are presented in Table 3, and a review of the distribution of the various different types of iridoids and cornoside found in species of Veronica, using our present results and those of previous investigations, is given in Table 4. During the compilation of data, it was noted that at least one species of 11 of the 13 subgenera had been investigated previously. The small subgenus Triangulicapsula, containing only two species, was the only subgenus for which no chemical results were available. Since no previous isolation of iridoids had been reported from subgenus Pseudolysimachium, we also examined Veronica longifolia from this taxon in the present work. Surprisingly, the two fairly large Australian and New Zealand subgenera Derwentia and Hebe had not been subjected to much chemical work, except for their content of flavonoids (c.f. Mitchell et al., 2001). However, chromatographic data on iridoids for these taxa were available, and for completeness, we decided to include these results in the analysis. From the listing in Table 4, it appears that the genus is fairly homogeneous. A general Veronica species contains the iridoid glucosides aucubin (5) and/or catalpol (6) as well as one or more 6-O-esters of catalpol (6ae6j). In addition some of the species contain one or more of the carboxylated iridoids epiloganic acid (9),
S.R. Jensen et al. / Biochemical Systematics and Ecology 33 (2005) 1031e1047
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gardoside (10), mussaenosidic acid (11), geniposidic acid (12) or esters of these, compounds (11 and 12) involved in or derived from the biosynthesis of aucubin and catalpol (c.f. Rønsted et al., 2003). Of these, mussaenoside, the methyl ester of 11, is apparently characteristic for subg. Veronica, but it is not confined to this subgenus. Finally, the distinctive iridoids with an 8,9-double bond (13e15) that seem to be characteristic for Plantaginaceae (Rønsted et al., 2003; Albach et al., 2004d) are present in a few of the species. These compounds are usually acids and either difficult to isolate and characterize or they are present in small amounts, and they may therefore have been overlooked in some investigations. Two subgenera appear unusual in either being heterogeneous and having unusual compounds present (Pocilla), or being almost devoid of iridoid glucosides which to some extent are replaced by cornoside (2) (Chamaedrys), and we will discuss these two taxa separately in the light of the DNA-sequence results (Albach et al., submitted for publication).
3.1. Iridoids in subgenus Pocilla This subgenus appears to consist of three clades (Albach et al., submitted for publication) corresponding to the subsections Pocilla (Agrestes-Gruppe sensu Lehmann, 1908), Biloba sensu Stroh (1942) and Subracemosae (incl. subsect. Brevistylae) sensu Elenevsky (1977). Chemically, Pocilla is the only subgenus really variable within Veronica, and with the limited data available we can distinguish three groups here, completely in agreement with the phylogram. The largest clade consists of subsection Pocilla (Albach et al., submitted for publication) of which three species have been investigated chemically (Veronica filiformis, Veronica persica and Veronica polita) and this section is phytochemically completely normal in iridoid content. The sister clade to Pocilla constitutes subsection Biloba (Albach et al., submitted for publication), one of the main subjects of the present work. From this subsection, three species have been investigated (Veronica argute-serrata, Veronica biloba and Veronica campylopoda). Surprisingly, only one of these species contains a 6-O-ester of catalpol; on the other hand, all three species possess the iridoid glucosides ajugol (7). The biosynthesis of ajugol has not been investigated, but it is most likely derived from mussaenosidic acid (11), which could be converted to 7 in two steps by decarboxylation and oxidation. Ajugol has not previously been reported from Veronica or from the tribe Veroniceae. In Plantaginaceae it is known from Angelonia integerrima (von Poser et al., 1997), Ourisia racemosa (Nicoletti et al., 1988) and from three species of Penstemon (Junior, 1983; Foderaro and Stermitz, 1992; AbdelKader and Stermitz, 1993). Elsewhere, it is very common in Lamiaceae (including Stachys; Meremeti et al., 2004) and it occurs sporadically in most families of Lamiales. Ajugol is not a major component in members of section Biloba, but it appears to be a useful marker for this subsection. The last clade in subgenus Pocilla is made up of V. intercedens, Veronica rubrifolia and their relatives (subsection Subracemosae; Albach et al., submitted for publication). Of these, only the former has been investigated (Albach et al., 2003)
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S.R. Jensen et al. / Biochemical Systematics and Ecology 33 (2005) 1031e1047
GlcO
GlcO OH
HO
HO
OH
O
HO
2; Cornoside
OH
3; Salidroside
OH OH
OH 1; Mannitol
2
O
HO
HO O
O
Cornoside aglucone O HO
OH
Rengyolone
O OH
O
O RO
OR'
HO 4 R=Rha, R'=H; Verbascoside 4a R=Rha, R'=Glu; Verpectoside B HO
HO
OH
HO
HO
OR
6
O HO
OGlc
O
O HO
5; Aucubin
HO
OGlc
6; Catalpol
OGlc
7; Ajugol
COOH HO
O
O
O R'O
8 R=Glc, R'=H; Melittoside 8a R=H, R'=Benzoyl; Globularifolin COOH
COOH HO
OGlc
O OGlc
O HO
RO 10; Gardoside
9; Epiloganic acid
O HO
OGlc
OGlc
11; Mussaenosidic acid
O OGlc COOH
6a R=benzoyl; Veronicoside 6b R=p-OH-benzoyl; Catalposide 6c R=3,4-di-OH-benzoyl; Verproside 6d R=vanilloyl; Amphicoside 6e R=isovanilloyl 6f R=veratroyl 6g R=caffeoyl; Verminoside 6h R=isoferuloyl; Minecoside 6i R=Glu-caffeoyl; Speedoside 6j R=Glu-feruloyl; Welloside
COOH
O HO
OGlc
12; Geniposidic acid
O R
OGlc
13 R=H; Anagalloside 14 R=OH; Arborescosidic acid 15 R=CH3COO; Alpinoside
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Table 3 Compounds detected in or isolated from extracts of Veronica species Species
Details of extract
Compounds detected by NMR
V. arvensis (Japan)
(a) Fresh aerial parts (ca. 3 g) extracted with 25 ml water of ambient temp. (b) Fresh aerial parts (ca. 3 g) extracted with 25 ml of hot water (70e90 ) Fresh whole plants (39 g) extracted with 200 ml hot EtOH and blended; 1.10 g of crude extract
(a) Cornoside aglucone and rengyolone (2:1) (b) Cornoside, small amount of iridoid (d 6.2) and some verbascoside-like compounds
Chromatography gave 0.3 g carbohydrate with 75% mannitol (1), 660 mg cornoside (2, 2%), 10 mg impure ajugol (7), 60 mg salidroside (3), 80 mg mixture of verbascoside-like compounds V. chamaedryoides Herbarium sample (45 mg), Mainly verbascoside-like compounds; some 50 ml EtOH iridoid (signal at ca. 6.2 ppm); no cornoside V. chamaedrys Frozen whole plants (55 g) Chromatography gave 0.6 g carbohydrate with 50% mannitol (1), 30 mg cornoside extracted with 200 ml EtOH; 1.71 g of crude extract aglucone, 70 mg rengyolone V. dillenii Herbarium sample (39 mg), Verbascoside (4) and cornoside (2) 50 ml EtOH V. laxa Herbarium sample (80 mg), No solubles detectable 50 ml EtOH V. magna Herbarium sample (43 mg), Only verbascoside-like compounds 50 ml EtOH V. micans Herbarium sample (44 mg), Mainly Verbascoside (4) and 50 ml EtOH some cornoside (2) V. micrantha Herbarium sample (111 mg), Only verbascoside-like compounds (1996) 50 ml EtOH V. micrantha Fresh aerial parts dried at Chromatography gave 90 mg carbohydrate (2004) 100 (8.0 g) blended in with 50% mannitol (1), 50 mg aucubin (5), 50 ml hot EtOH; 630 mg 9 mg verpectoside B (4a). The main fraction of crude extract (300 mg) eluted at the end with 100% MeOH consisted probably of triterpene glycosides V. orbelica Herbarium sample (35 mg), Only verbascoside-like compounds 50 ml EtOH V. verna Herbarium sample (57 mg), Cornoside (2) was the main constituent 50 ml EtOH V. vindobonensis Herbarium sample (39 mg), Verbascoside (4) and cornoside (2) 50 ml EtOH V. argute-serrata Fresh whole plants (189 g) Chromatography gave 1.3 g carbohydrate (IOK-3/2003) blended in 500 ml EtOH; with 90% mannitol (1), 50 mg catalpol (6), 220 mg 2.86 g of crude extract aucubin (5), 20 mg gardoside (10), 30 mg ajugol (7), 10 mg mussaenosidic acid (11), 30 mg epiloganic acid (9), 10 mg arborescosidic acid (14), 50 mg verbascoside-like compounds, 60 mg of a fraction with an unidentified acetyl-flavone glycoside V. argute-serrata Fresh whole plants Chromatography gave 1.8 g carbohydrate with (IOK-4/2003) (216 g) blended in 500 90% mannitol (1), 80 mg catalpol (6), 175 mg ml EtOH; 2.67 g aucubin (5), 15 mg gardoside (10), 10 mg ajugol of crude extract (7), 5 mg mussaenosidic acid (11), 45 mg epiloganic acid (9), 22 mg arborescosidic acid (14), 60 mg of a fraction with an unidentified acetyl-flavone glycoside V. arvensis (Denmark)
(continued on next page)
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Table 3 (continued ) Species
Details of extract
Compounds detected by NMR
V. biloba
Fresh whole plants (79 g) blended in 300 ml EtOH; 1.44 g of crude extract Fresh whole plants (203 g) blended in 800 ml EtOH; 2.80 g of crude extract
Chromatography gave carbohydrate fraction (not examined), 25 mg catalpol (6), 110 mg aucubin (5), 25 mg ajugol (7), 5 mg epiloganic acid (9), 10 mg alpinoside (15) Chromatography gave 1.8 g carbohydrate with 90% mannitol (1), 140 mg catalpol (6), 100 mg aucubin (5), 10 mg ajugol (7), 10 mg verminoside (6g), 70 mg of a fraction with an unidentified acetyl-flavone glycoside Chromatography gave 0.9 g carbohydrate with 25% mannitol (1), 40 mg catalpol (6), 5 mg aucubin (5), 370 mg verproside (6c), 60 mg catalposide (6b), 50 mg verminoside (6g), 80 mg of a catalpol ester mixt., 50 mg flavones
V. campylopoda
V. longifolia
Fresh aerial parts (70 g) blended in 300 ml EtOH; 2.09 g of crude extract
and with regard to iridoid content this species is one of the most aberrant known so far in lacking aucubin and catalpol but containing the 5-hydroxylated iridoids melittoside (8) and globularifolin (8a). Like ajugol, melittoside is common in Lamiaceae (including Stachys; Meremeti et al., 2004), but it has never been reported from Veronica or even from Veroniceae, although it is known from some species of Plantago (Rønsted et al., 2003) and from Campylanthus (Rønsted and Jensen, 2002). Globularifolin is more rare; it was first isolated from Globularia cordifolia (Chaudhuri and Sticher, 1980a) and Melampyrum sylvaticum (Chaudhuri and Sticher, 1980b) and is also known from Plantago media (Saadi et al., 1990). The presence of 8 and 8a in V. intercedens is remarkable, because this species possesses the defining morphological characters of the subgenus (pairwise fusion of the calyces, more or less recurved pedicels when fruiting, mostly strongly bilobed capsules). Analyses of more members of the subgenus, particularly V. rubrifolia, seem warranted. 3.2. Cornoside in subgenus Chamaedrys Half of the investigated species in Chamaedrys contained the phenylethanoid glucoside, cornoside (2), in the other half of the species neither 2 nor any substantial amounts of iridoids seemed to be present, although closer investigation of two species revealed that a trace of ajugol was present in one species and some aucubin in another. The presence of cornoside is reported here for the first time in Veronica and it appears to be confined to subgenus Chamaedrys as defined by Albach et al. (2004c) (see also Albach et al., submitted for publication). Ajugol (7) was also isolated during the preparative work-up of Veronica arvensis, but the amount was very small (!2%) compared to the quantity of cornoside found in the plant, and it would not have been discovered in the smaller samples (from herbarium specimens) used for most of the other species investigated. In the initial experiments we used herbarium specimens, and the stability of cornoside in such specimens or in frozen samples may pose
Table 4 Iridoid glucosides isolated from Veronica (sensu Albach et al., 2004c) species Species
Subgenus
(5/6)b
6-O-esters of catalpolc
11-COOR (9e12)d
V. alpina
Veronica
5, 6
11
Taskova et al., 1998
V. bellidioides
Veronica
5, 6
11, 12
Taskova et al., 1998
V. officinalis V. anagallisaquatica V. undulata Veronica longifolia V. besseya (Z Besseya alpina) V. plantaginea (Z B. plantaginea) V. cymbalaria V. hederifolia V. triphyllos V. kelleri
Veronica Beccabunga
5, 6 5, 6
Beccabunga Pseudolysimachium Synthyris
n.i. 5, 6 5, 6
6a, 6h, 6a, 6h, 6a, 6a, 6d, 6a, 6b, 6a,
Synthyris
6
6a, 6c, 6e
Cochlidiosperma Cochlidiosperma Pellidosperma Stenocarpon
5, 6 5 5, 6 5, 6 n.i.
V. intercedens V. filiformis
Stenocarpon Triangulicapsula Pocilla Pocilla
6c, 6d, 6f, 6g 6a, 6b, 6d, 6g 6d 6a, 6b, 6c, 6d, 6f, 6g 6b, 6c, 6d, 6e, 6f
e 5, 6
V. persica
Pocilla
5, 6
V. polita (Z V. didyma) V. argute-serrata V. biloba
Pocilla
5
e 6a, 6d, 6a, 6d, 6b,
Pocilla Pocilla
5, 6 5, 6
e e
11, 11e 9e, 10e, 11, 12e
13
e
e
C6eC2g
e
Reference
Afifi-Yazar and Sticher, 1980 Lahloub, 1992b; Lahloub et al., 1993; Su et al., 2000; Harput et al., 2004 Aoshima et al., 1994 this work Gardner et al., 1987
Gardner et al., 1987
9, 11
Taskova et al., 1999 Harput et al., 2002b Grabias et al., 1995 Taskova et al., 1998
15 9 12
Gao et al. (2003) e
8, 8a
e
6b, 6c, 6g, 6h 6b, 6c, 6f, 6g 6c, 6d
Albach et al., 2003 Lahloub, 1992a Lahloub et al., 1991; Harput et al., 2002a Tomassini et al., 1995, Wang et al., 1995
7, 14 7, 15
e e
this work this work (continued on next page)
1041
9, 10, 11 9
S.R. Jensen et al. / Biochemical Systematics and Ecology 33 (2005) 1031e1047
V. ciliata
6b, 6d, 6i 6b, 6d, 6i, 6j 6c, 6g, 6h 6b, 6c, 6g, 6h 6c, 6g, 6h 6c, 6h 6c, 6e
Other iridoidsf
(5/6)b
6-O-esters of catalpolc
V. V. V. V. V. V. V. V. V.
Pocilla Pentasepalae Pentasepalae Pentasepalae Pentasepalae Pentasepalae Pentasepalae Chamaedrys Chamaedrys
5, 6 6 6 6 5 5, 6 5, 6 e
6h 6c, 6e, 6f, 6g 6c 6c, 6d, 6f 6h 6a, 6b, 6c, 6d, 6f 6a, 6c, 6d, 6f, 6g e
e
7
Chamaedrys Chamaedrys Chamaedrys Chamaedrys Chamaedrys Chamaedrys Chamaedrys Chamaedrys Chamaedrys
e
e
e
e
5
e
e
e
Derwentia Hebe
5, 6 5, 6
present present
? ?
? ?
campylopoda fuhsii liwanensis multifida orientalis pectinata thymoides arvensis chamaedryoides (NMR)a V. chamaedrys V. dillenii (NMR)a V. laxa (NMR)a V. magna (NMR)a V. micans (NMR)a V. micrantha V. orbelica (NMR)a V. verna (NMR)a V. vindobonensis (NMR)a 2 Species (chrom)a Many species (chrom)a a
11-COOR (9e12)d
Other iridoidsf
C6eC2g
Reference
7
e
2, 3 e
this work O¨zipek et al., 1998, 2000a Albach et al., 2003 O¨zipek et al., 2000b Albach et al., 2003 Harput et al., 2003 Varel, 2004 this work this work
2 2 e e 2 e e 2 2
this this this this this this this this this
? ?
Grayer-Barkmeijer, 1979 Grayer-Barkmeijer, 1979
e e
work work work work work work work work work
Quantitative data do not exist. Presence of aucubin (5) and catalpol (6). c Veronicoside (6a), catalposide (6b), verproside (6c), amphicoside (6d), isovannilloyl-catalpol (6e), veratroyl-catalpol (6f), verminoside (6g), minecoside (6h), speedoside (6i), welloside (6j). d Epiloganic acid (9), gardoside (10), mussaenosidic acid (11), geniposidic acid (12) or an ester of these. e Shanzhiside methyl ester and bochnaloside was also found in V. anagallis-aquatica. f Ajugol (7), melittoside (8), globularifolin (8a), anagalloside (13), arborescosidic acid (14), alpinoside (15). g Cornoside (2), salidroside (3). b
S.R. Jensen et al. / Biochemical Systematics and Ecology 33 (2005) 1031e1047
Subgenus
1042
Table 4 (continued ) Species
S.R. Jensen et al. / Biochemical Systematics and Ecology 33 (2005) 1031e1047
1043
a problem. When plants are pressed and still moist, enzymes can degrade the compound during drying. And with freezing, cell walls become degraded and the enzymes get in contact with the glycosides to cause hydrolysis of the glycoside bond. That this may indeed be the case is demonstrated by our experiments. When extracting a larger amount of frozen V. chamaedrys by blending with cold ethanol, we could isolate only cornoside aglucone and rengyolone. We had a similar experience with V. arvensis. Thus, extraction of a fresh plant with cold water produced an extract containing a mixture of cornoside aglucone and rengyolone. Conversely, doing the extraction with hot water, which deactivates the glucosidase, we obtained an extract with intact cornoside present. Following this lead, we worked up a larger amount of fresh V. arvensis by extraction with boiling ethanol and were able to isolate the intact cornoside in considerable amount (2% of fresh weight). In the case of V. chamaedrys, it is not clear whether the degradation of cornoside had taken place during freezing or during work-up. Regarding the stability of 2 in herbarium specimens, it should be noted that in the three cases where cornoside was actually detected in herbarium specimens, it was intact. Furthermore, in the case of V. micrantha, where no 2 could be detected in the herbarium sample, it was also absent in the freshly dried sample; however, from the latter a significant amount of aucubin could be isolated, together with the phenylethanoid triglycoside verpectoside B (4a), previously reported only from Veronica pectinata (Saracoglu et al., 2002). Cornoside has apparently been overlooked in previous studies of Veronica, because it may not react with the specific iridoid reagents used for paper chromatography or TLC. Besides, no standards of cornoside were available during these surveys. It is noteworthy that iridoids are lacking or only present in small amounts in all members of the subgenus. Mutual exclusion is found among many of the cornoside-containing genera and families as first noted by Jensen (1992). 3.3. Distribution of cornoside in plants Cornoside (2) is a phenylethanoid glucoside known to be biosynthesized from salidroside (3) (Eigtved et al., 1976; Yamamoto et al., 2003) and is likely to belong to the same C6eC2 pool that gives rise to verbascoside (5). Rengyolone (Z halleridone) is usually co-occurring with 2 and can be considered an artifact formed from cornoside aglucone either in vivo or during work-up of the plant material (c.f. Bianco et al., 1993). Cornoside is a compound with a limited distribution in plants (Jensen, 1992); it was initially found in many species of Cornus (Jensen et al., 1973, 1975a), but apart from two findings from Eurya (Theaceae; Inada et al., 1989; Khan et al., 1992), it is so far only known from Lamiales where it is a characteristic for the tribe Forsythieae (Abeliophyllum, Forsythia) in Oleaceae (Jensen et al., 2002) but it also is known from Olea europea (Bianco et al., 1993). It has been found in four members of the family Gesneriaceae (Jensen, 1996) as well as in both species investigated from Tetrachondraceae (Jensen, 2000). In Bignoniaceae, it is known from Eccremocarpus (von Poser et al., 2000), Millingtonia (Hase et al., 1995), Oroxylum (Teshima et al., 1996) and Tecoma (Guiso et al., 1997) and also in Barnettia and Markhamia as the hydrogenated form, rengyoside B (Kanchanapoom
1044
S.R. Jensen et al. / Biochemical Systematics and Ecology 33 (2005) 1031e1047
et al., 2002a,b). Otherwise, it has been reported from Digitalis (Jensen et al., 1975b) and Isoplexis (as halleridone; Llera et al., 1987) of Plantaginaceae, from Clerodendrum (as halleridone; Tian et al., 1997) and from Teucrium (Bellakhdar et al., 1988) of Lamiaceae, Phyla (Verbenaceae; Rimpler and Sauerbier, 1986), Martynia (Martyniaceae; Sasaki et al., 1978), Halleria (Stilbaceae; Messana et al., 1984), Calceolaria (Calceolariaceae; Nicoletti et al., 1988) and from Plocosperma (Plocospermataceae; Jensen, 1992). When cornoside was first discovered in Cornus (Jensen et al., 1973, 1975a), the distribution was confined to the species (subg. Mesomora and Craniopsis) that do not contain iridoids and this is completely consistent with the DNA-sequence results (Fan and Xiang, 2001); and it is remarkable that in most other cases where cornoside has been found, the source plant does not contain iridoids even if related species are known to do so. Exceptions to this trait among the above taxa are some of those of Bignoniaceae and Lamiaceae as well as Martynia and Olea. In comparison with published DNA-based phylogenies (Oxelman et al., 1999; Olmstead et al., 2001), it is noteworthy that cornoside seems especially frequent in the first-branching families of Lamiales (Plocospermataceae, Oleaceae, Tetrachondraceae, Gesneriaceae, Calceolariaceae), but scattered to absent in most other families. In those instances such as here in Veronica, it thus seems to be a reversal to an ancestral condition.
Acknowledgements We thank the staff of The Botanic Garden, The University of Copenhagen, and Dr. M. Montserrat Martı´ nez-Ortega for providing plant material. FWF (Fonds zur Fo¨rderung der wissenschaftlichen Forschung) project P15336 is gratefully acknowledged for financial support for traveling costs. References Abdel-Kader, M.S., Stermitz, F.R., 1993. Chemistry of the Scrophulariaceae. Part 28. Iridoid and other glycosides from Penstemon species. Phytochemistry 34, 1367e1371. Afifi-Yazar, F.U., Sticher, O., 1980. Verproside, a new iridoid glucoside from Veronica officinalis L. (Scrophulariaceae). Helv. Chim. Acta 63, 1905e1907. Albach, D.C., Chase, M.W., 2001. Paraphyly ofVeronica based on sequences from the internal transcribed spacers (ITS) of nuclear ribosomal DNA. J. Plant Res. 114, 9e18. Albach, D.C., Grayer, R.J., Jensen, S.R., Ozgokce, F., Veitch, N.C., 2003. Acylated flavone glycosides from Veronica. Phytochemistry 64, 1295e1301. Albach, D.C., Martı´ nez-Ortega, M.M., Chase, M.W., 2004a. Veronica: parallel morphological evolution and phylogeography in the Mediterranean. Plant Syst. Evol. 246, 177e194. Albach, D.C., Martı´ nez-Ortega, M.M., Fischer, M.A., Chase, M.W., 2004b. Evolution of Veroniceae: a phylogenetic perspective. Ann. Mo. Bot. Gard. 91, 275e302. Albach, D.C., Martı´ nez-Ortega, M.M., Fischer, M.A., Chase, M.W., 2004c. A new classification of the tribe Veroniceae e problems and a possible solution. Taxon 53, 429e452. Albach, D.C., Gotfredsen, C.H., Jensen, S.R., 2004d. Iridoid glucosides of Paederota lutea and the relationships between Paederota and Veronica. Phytochemistry 65, 2129e2134.
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Albach, D.C., Jensen, S.R., O¨zgo¨kce, F., Grayer, R.J., Veronica: chemical characters for the support of phylogenetic relationships based on nuclear ribosomal and plastid DNA sequence data. Biochem. Syst. Ecol., submitted for publication. Aoshima, H., Miyase, T., Ueno, A., 1994. Phenylethanoid glycoside from Veronica undulata. Phytochemistry 36, 1157e1158. Bellakhdar, J., De la Torre, M.C., Rodriguez, B., Savona, G., Bruno, M., Piozzi, F., 1988. Halleridone and related products from Teucrium decipiens. Planta Med. 54, 267. Bentham, G., 1846. Scrophulariaceae. In: de Candolle, A. (Ed.), Prodromus systematis naturalis regni vegetabilis, vol. 10. Victor Masson, Paris, pp. 448e491. Bianco, A., Lo Scalzo, R., Scarpati, M.L., 1993. Isolation of cornoside from Olea europea and its transformation into Halleridone. Phytochemistry 32, 455e457. Bock, K., Pedersen, C., 1983. Carbon-13 nuclear magnetic resonance spectroscopy of monosaccharides. Adv. Carbohydr. Chem. Biochem. 41, 27e66. Chaudhuri, R.K., Sticher, O., 1980a. Glycosides of Globulariaceae. Part 3. Globularifolin, a new acyl iridoid glucoside from Globularia cordifolia. Helv. Chim. Acta 63, 117e120. Chaudhuri, R.K., Sticher, O., 1980b. Minor iridoid glucosides of Melampyrum silvaticum. Planta Med. 39, 140e143. Eigtved, P., Jensen, O.S., Kjaer, A., Wieczorkowska, E., 1976. Biosynthesis of a quinol glucoside in Cornus. Acta Chem. Scand. B30, 182e184. Elenevsky, A.G., 1977. Sistema roda Veronica L. Byull. Mosk. O-Va. Ispyt. Prir. Otd. Biol. 82, 149e160. Fan, C., Xiang, Q.-Y., 2001. Phylogenetic relationships within Cornus (Cornaceae) based on 26S rDNA sequences. Am. J. Bot. 88, 1131e1138. Foderaro, T.A., Stermitz, F.R., 1992. Chemistry of the Scrophulariaceae. Part 24. Iridoid glycosides from Penstemon species: a C-5,C-9 trans iridoid and C-8 epimeric pairs. Phytochemistry 31, 4191e4195. Gao, K., Li, X., Liu, A., Jia, Z., 2003. Chemical constituents of Veronica ciliate, as a psychrophyte from Northwest China. Xibei Zhiwu Xuebao 23, 633e636 (Chem. Abstr. 2004, 618033). Gardner, D.R., Narum, J., Zook, D., Stermitz, F.R., 1987. Chemistry of the Scrophulariaceae. Part 9. New iridoid glucosides from Castilleja and Besseya: 6-hydroxyadoxoside and 6-isovanillylcatalpol. J. Nat. Prod. 50, 485e489. Grabias, B., Ofterdinger-Daegel, S., Swiatek, L., 1995. Iridoids and phenolic acids in Veronica triphyllos L. Herba Pol. 41, 115e119. Grayer, R.J., Chase, M.W., Simmonds, M.S.J., 1999. A comparison between chemical and molecular characters for the determination of phylogenetic relationships among plant families: an appreciation of Hegnauer’s ‘‘Chemotaxonomie der Pflanzen’’. Biochem. Syst. Ecol. 27, 369e393. Grayer-Barkmeijer, R.J., 1973. A chemotaxonomic study of Veronica: iridoid glucosides. Biochem. Syst. Ecol. 1, 101e110. Grayer-Barkmeijer, R.J., 1979. Chemosystematic investigations in Veronica L. (Scrophulariaceae) and related genera. PhD Thesis, University of Leiden. Guiso, M., Marra, C., Piccioni, F., Nicoletti, M., 1997. Iridoid and phenylpropanoid glucosides from Tecoma capensis. Phytochemistry 45, 193e194. Harput, U.S., Saracoglu, I., Inoue, M., Ogihara, Y., 2002a. Phenylethanoid and iridoid glycosides from Veronica persica. Chem. Pharm. Bull. 50, 869e871. Harput, U.S., Saracoglu, I., Nagatsu, A., Ogihara, Y., 2002b. Iridoid glucosides from Veronica hederifolia. Chem. Pharm. Bull. 50, 1106e1108. Harput, U.S., Nagatsu, A., Ogihara, Y., Saracoglu, I., 2003. Iridoid glucosides from Veronica pectinata var. glandulosa. Z. Naturforsch. C 58, 481e484. Harput, U.S., Varel, M., Nagatsu, A., Saracoglu, I., 2004. Acylated iridoid glucosides from Veronica anagallis-aquatica. Phytochemistry 65, 2135e2139. Hase, T., Kawamoto, Y., Ohtani, K., Kasai, R., Yamasaki, K., Picheansoonthon, C., 1995. Cyclohexylethanoids and related glucosides from Millingtonia hortensis. Phytochemistry 39, 235e241. Inada, A., Fujiwara, M., Kakimoto, L., Kitamura, F., Toya, H., Konishi, M., 1989. Structure of a new acylated flavonoid glycoside, euryanoside, from flowers of Eurya japonica Thunb. Chem. Pharm. Bull. 37, 2819e2821.
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