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Iridoids in Hydrangeaceae
Gousiadou, Chryssoula; Li, Hong-Qing; Gotfredsen, Charlotte Held; Jensen, Søren Rosendal
Published in:Biochemical Systematics and Ecology
Link to article, DOI:10.1016/j.bse.2015.12.002
Publication date:2016
Document VersionPeer reviewed version
Link back to DTU Orbit
Citation (APA):Gousiadou, C., Li, H-Q., Gotfredsen, C. H., & Jensen, S. R. (2016). Iridoids in Hydrangeaceae. BiochemicalSystematics and Ecology, 64, 122-130. https://doi.org/10.1016/j.bse.2015.12.002
1
Iridoids in Hydrangeaceae
Chrysoula Gousiadoua, Hong-Qing Li
b, Charlotte Gotfredsen
a, Søren Rosendal Jensen
a,*
aDepartment of Chemistry, Technical University of Denmark, DK-2800, Lyngby, Denmark
bSchool of Life Sciences, East China Normal University, Shanghai, China
Abstract
* Corresponding author. Tel.: +45-45252103; fax: +45-45933968.
E-mail address: srj@kemi.dtu.dk (S.R. Jensen).
2
The content of glycosides in Kirengeshoma palmata and Jamesia americana
(Hydrangeaceae) have been investigated. The former contains loganin and
secoiridoids, including the alkaloid demethylalangiside. The latter contains no
iridoids, but the known glucosides arbutin, picein and prunasin. In order to futher
investigate the chemotaxonomy of the family Hydrangeaceae, the distribution of the
iridoid and secoiridoid glucosides as well as the known biosynthetic pathways to these
compounds have been reviewed. However, only a few genera of the family has been
investigated. Loganin, secologanin, and derivatives of these are common. The genus
Deutzia is characteristic in containing more structurally simple iridoids in which C-10
has been lost during biosynthesis. Such compounds have so far only been reported
from the genus Mentzelia (Loasaceae). The taxonomic relationships between
Hydrangeaceae and the closely related Cornaceae and Loasaceae is discussed and
found to agree well with recent DNA sequence results.
Keywords:
Kirengeshoma
Jamesia
Hydrangeaceae
Iridoid glycosides
Chemotaxonomy
3
1. Introduction
de Jussieu (1789) originally placed Hydrangeaceae in Saxifragaceae and this
association was followed by most taxonomists (Bentham and Hooker, 1862-83;
Engler, 1928; Takhatajan, 1969; 1980; Cronquist, 1988). Dahlgren (1975; 1980;
1989), who put a great weight on embryology was impressed by the correlation with
the occurrence of iridoid compounds, and he was one of the first to place the family in
his Cornales. Thorne (1992) and Hufford (1992) followed this concept, and with the
advent of DNA sequencing techniques (Downie and Palmer, 1992; Hufford et al.,
2001; Albach et al., 2001) Loasaceae was also placed in Cornales. The relationships
between the genera of Hydrangeaceae has primarily been analyzed by Hufford (1997;
Hufford et al., 2001). The DNA sequencing phylogenetic relationships are depicted in
Fig. 1.
Only the genera Hydrangea and Deutzia appears to have been much investigated
chemically, probably due the common use of these two genera as garden ornamentals.
The family consists of 17 genera in the two subfamilies (Hufford et al., 2001):
Hydrangeoideae, include tribe Hydrangeeae (Hydrangea, Platycrater, Decumaria,
Pileostegia, Schizophragma, Dichroa, Broussaisia, Deinanthe, Cardiandra) and
tribes Philadelpheae (Philadelphus, Carpenteria, Deutzia, Kirengeshoma, Whipplea,
Fendlerella), and Jamesioideae (Fendlera, Jamesia). In order to extend these studies
we have investigated a member of each of the last two tribes, namely Kirengeshoma
palmata Yatabe and Jamesia americana Torr. & A. Gray .
2. Materials and Methods
2.1 Plant material
Fresh material of Kirengeshoma palmata from two different plants (IOK 8-1999 and
IOK 1-2010) and Jamesia americana (IOK 13-2003) was provided by the staff of the
Botanical Garden of The University of Copenhagen. The vouchers were authenticated
by one of us (HQL) and deposited in the herbarium of East China Normal University
(HSNU).
2.2. General
1H,
13C spectra were recorded 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. Preparative HPLC was performed on a
Merck Lobar RP-18 column size B or C.
2.3. Extraction and isolation
2.3.1 Kirengeshoma palmata
a) Fresh, aerial parts collected in June (65 g) were blended with EtOH (300 ml),
filtered and taken to dryness. Partitioning in H2O-Et2O gave from the aq. phase after
drying 2.5 g which was chromatographed on a C column to give in order of elution:
chlorogenic acid (5, 250mg); salidroside (80 mg); 6--hydroxysweroside (3, 22 mg);
sweroside (2, 740 mg); loganin (1, 80 mg).
b) Fresh, frostbitten aerial parts collected in October (58 g) were cut into small pieces,
blended with EtOH (250 ml), boiled for 10 min and left to extract overnight. The
extract was filtered, dried (3.05 g) and partitioned in H2O-Et2O (2:5). The aq. phase
4
was collected, dried (1.70g) and subsequently subjected to preparative
chromatography. The initial solvent used was H2O, then mixtures of H2O-MeOH of
decreasing polarity, and finally MeOH. The following compounds were obtained in
order of elution: chlorogenic acid (5, 120mg); 6--hydroxysweroside (3, 20 mg);
sweroside (2, 70 mg); loganin (1, 80 mg) and fraction A (50 mg) was obtained.
Fraction A was further purified using the solvent mixture (2:1) to yield
demethylalangiside (4, 10 mg).
2.3.2 Jamesia americana
Frozen aerial parts (23 g) were blended with EtOH (150 ml). After filtering, the
extract was taken to dryness and partitioned in H2O-Et2O. The concentrated aq. phase
(1.50 g) was chromatographed as above to give: sugars (mainly glucose; 310 mg);
arbutin (6; 30 mg); picein (7; 35 mg) and prunasin (8; 150 mg).
2.3.3 Perspective and outline
In order to extend the results obtained from the two plants we have undertaken to
make a review of the iridoids reported from the Hydrangeaceae including the reported
data on the biosynthesis of the compounds found in the family. Furthermore, we have
discussed the distribution of relevant compounds in relation to the phylogenetic
results shown in the cladogram (Fig. 1).
3. Results and Discussion
The aqueous extract of the aerial parts of K. palmata after chromatography on
preparative reverse phase gave loganin (1) and three secoiridoids, namely sweroside
(2), 6-β-hydroxysweroside (3) (Rodríguez et al., 2002) and demethylalangiside (4)
(Itoh et al., 2001) as well as chlorogenic acid (5).
J. americana has been investigated by Plouvier (1959) who discovered the presence
of a cyanogenic glycoside. In the present work, we have isolated the compounds
Arbutin (6), picein (7) (Johansen et al., 2007) and prunasin (8) (Hübel et al,. 1981),
the latter is most likely the cyanogenic compound detected by Plouvier. No iridoids
were found.
The compounds isolated were identified by comparison with spectra of authentic
compounds or published data.
OH
OH
OGlc
N O
4 Demethyl- alangiside
O
OGlc
O O
OH
3 6-Hydroxysweroside
COOH
OH
O
OH
OH
O
OH
OH
5 Chlorogenic acid
O
GlcO
7 Picein
GlcO
OH
6 Arbutin
OGlc
CNH
8 Prunasin
O
OGlc
O O
2 Sweroside
O
OGlc
OH
COOMe
1 Loganin
5
3.1 Biosynthesis
3.1.1 Secoiridoids
The iridoids are of terpenoid origin and their biosynthesis (Fig. 2) has been well
investigated (Inouye et al., 1977a, Inouye and Uesato, 1986; Jensen, 1991, 1992),
although new information about the early steps have recently been discovered (Salim
et al., 2014; Miettinen et al., 2014).
Fig. 2. Biosynthesis of secologanin.
Thus, it has been shown that these compounds are not of mevalonoid origin as first
believed, but that they arise by the recently discovered triose phosphate/pyruvate
pathway via 1-deoxy-D-xylulose in Mentha (Eisenreich et al., 1997) and in Swertia
(Wang et al., 2001) in the case of geraniol. Using cell-free extracts from Lonicera
japonica Thunb. and Hydrangea macrophylla (Thunb.) Ser., it has furthermore been
shown that the initial glucosylation in the pathway take place in the formation of
deoxyloganic acid (11) (Yamamoto et al., 2002). Secologanin (14) has also been
shown to derive from the triose phosphate/pyruvate pathway in Catharanthus roseus
(L.) G. Don cell-cultures (Contin et al., 1998; Miettinen et al., 2014).
3.1.2 Ipecac alkaloids
A group of tetrahydroisoquinoline alkaloids of limited distribution are derived from
secologanin (14). This has been shown in Cephaelis ipecacuanha (Brot.) A. Rich.
O
OH
O
OH
CHO
O
OGlc
COOH
9 Iridodial 10 Iridotrial
11 Deoxyloganic acid
O
OGlc
OH
COOMe
O
OGlc
CHO COOMe
1 Loganin
14 Secologanin
tetrahydro- isoquinoline and complex indole alkaloids
CH3
O
OH H
OH
CH2OH
OH
Geraniol1-Deoxy-D-xylulose
O
OGlc
COOH
OH
12 Loganic acid
O
OGlc
OOH O
13 Secologanic acid
O
OGlc
O O
2 Sweroside
6
(Rubiaceae) by Battersby and Gregory (1968) where labelled loganin (1) was
incorporated in ipecoside (15) which is likely to be the precursor of the ipecac
alkaloids.
Fig. 3. Biosynthesis of ipecac alkaloids.
3.1.3 Deutzia iridoids
The iridoid glucosides found in Deutzia species are peculiar since they lack the C-10
carbon atom, a feature rarely seen in the compounds from other plants. The
biosynthesis (Inouye et al., 1977b, Uesato et al, 1986) is different from that above
(Fig. 4) since glucosylation apparently takes place earlier, namely at the iridodial
stage. Thus, it has been shown by feeding deuterium labelled precursors (Frederiksen
et al., 1999) to proceed from iridodial glucoside (9a) via decapetaloside (16) to the
compounds present in the plants, deutzioside (18) and scabroside (19). The compound
loasaside (17) has not been tested as an intermediate, but seems the logical step prior
to 18 and 19.
Fig. 4. Biosynthesis of Deutzia compounds.
3.2 Iridoids and some other glycosides in Hydrangeaceae
3.2.1 Hydrangeeae; Hydrangea
Loganin (1) was first reported (Plouvier, 1964) from three species of Hydrangea,
namely H. aspera D. Don, H. bretschneideri Dippel and H. xanthoneura Diels. This
compound has later been reported from H. hortensis Sm. (Khalifa et al., 2001) and H.
macrophylla (Yamamoto et al, 2002). Recently, the -glucopyranosyl ester of
deoxyloganic acid (11), namely 11a, was isolated from H. macrophylla subsp. serrata
(Thunb.) Makino (Kikuchi et al., 2008a).
O
OGlc
CHO COOMe
1
14 Secologanin
NH2
OH
OH
OH
OH NAc
OGlc
COOMe
15 Ipecoside
OO
OGlc
OHCH
3
18 Deutzioside
OO
OGlc
OH OHCH
3
19 Scabroside
O
OGlc
CH3
O
OGlc
OHCH
3
16 Decapetaloside
O
OGlc
CH3
OH
17 Loasaside9a Iridodial glucoside
7
Also, a number of aromatic esters of loganic acid (12) as well as loganin (1) and three
diglucosides of this has been reported from H. paniculata Sieb. (Shi et al., 2012).
Examples are (12a) and (1a).
Loganin (1), secologanic acid (13), secologanin (14) and sweroside (2) as well as four
derivatives of (14) named hydrangeosides A-D (20-23) were found in H. macrophylla
var. macrophylla (Inouye et al., 1980; Uesato et al., 1981).
A year later, three similar compounds, namely hydrangeosides E-F (24-26) were
reported from H. scandens (L. f.) Ser. (Uesato et al., 1982). In addition, in a final
paper (Uesato et al., 1984) the absolute structures of the seven compounds (20-26)
were elucidated. Hydrangeoside A (20) has also been reported from H. chinensis
Maxim. (Patnam et al., 2001), H. hortensis (Khalifa et al., 2001) together with the
dimethyl acetal of secologanin (14), a typical artifact formed from 14 when extracting
the plant material with methanol.
More recently, another variety of the plant, namely H. macrophylla var. thunbergii
Makino was investigated (Yoshikawa et al., 1994; Matsuda et al., 1999) to give the
somewhat different lactones hydramacroside A (27) and B (28). This study was later
O
OGlc
GlcO
COOMe
O
OGlc
COOH
O
OH O
MeOO
OGlc
COOGlc
11a 12a 7-Feruloylloganic acid 1a 7-OGlucopyranosyl -loganin
20 Hydrangeoside A
O
OGlc
COOMeOH
OH
O
O
OGlc
COOMeO
OH
O
O
H
26 Hydrangeoside G
O
OGlc
COOMe
OH
OH
O
H
24 Hydrangeoside E
O
OGlc
COOMe
OH
OH
O
H
25 Hydrangeoside F
21 Hydrangeoside B
O
OGlc
COOMeO
OH
O
O
H
O
OGlc
COOMe
OH
O
O
H
23 Hydrangeoside D
O
OGlc
COOMe
OH
O
O
H
22 Hydrangeoside C
8
extended by an investigation of the flowers of the same variety and gave
hydrangeoside A (20) as well as 27 and 28, and in addition the two alkaloids derived
from 28, namely the two epimers hydrangeamine A (29) and B (30) (Liu et al., 2013).
From a third taxon, H. macrophylla subsp. serrata was isolated hydrangeoside A (20)
and C (22) as well as the dimethyl acetal of 20 and a number of methyl and/or n-butyl
acetal derived from secologanin (14), secologanic acid (13) or morroniside (31)
(Sakai et al., 2007; Kanno et al., 2007). Such acetals are usually artifacts formed with
the solvents used during work-up. Further work with this plant provided the four
macropyllanosides A-D (32-35), cyclic acetals of 14 with glycerol D-
galactopyranoside, myo-inositol and shikimic acid (Kikuchi et al., 2008b).
An additional acetal of secologanin, this time with the cyanogenic glucoside
taxiphyllin, namely hydracyanoside D (36), was later reported from the parent H.
macrophylla (Wang et al., 2010) together with hydracyanoside F (37), secoxyloganin
(38) and 8-epiloganin (39).
27 Hydramacroside A 28 Hydramacroside B
O
OGlc
O O
OOH
OH
H
O
OGlc
O OH
OH
OOHO
29 Hydrangeamine A
N
O
OGlc
O OH
OH
30 Hydrangeamine B
N
O
OGlc
O OH
OH
O
OGlc
COOMe
O
OH
31 Morroniside 32 Macrophyllanoside A (R=Glyceryl)
O
OGlc
COOMeOO
HOOC
OH
H
O
OGlc
COOMeOO
H
OH
OHOH
OH
33/34 Macrophyllan- osides B and C
35 Macrophyllan- oside D
O
OGlc
COOMeO
OOH
OH
OOR
9
Finally, two esters of demethylsecologanol were isolated from H. paniculata (Shi et
al., 2014), namely hydrangeside B (40a) and methylgrandifloroside (40b).
3.2.2 Hydrangeeae; Others
Platycrater, Decumaria, Pileostegia, Broussaisia, Deinanthe, Cardiandra appears not
to have been properly investigated; of these, Decumaria and Broussaisia have only
been examined for flavonoids (Bohm et al, 1985). Dichroa febrifuga Lour., on the
other hand, is much used in Chinese medicine and has been well investigated.
However, no iridoids have been reported.
3.2.3 Philadelpheae; Deutzia
The compound scabroside (19) was the first iridoid glucoside isolated from D. scabra
Thunb. (Esposito and Guiso, 1973), quickly followed by deutzioside (18) (Bonadies et
al., 1974) and deutziol (41) (Esposito et al., 1976). Later, work was continued on this
plant and gave rise to scabrosidol (42) (Esposito et al., 1983) and the two aglucones
deutziogenin (18a) and scabrogenin (19a) (Esposito et al., 1984). The compounds 18
and 19 have also been isolated from D. crenata Sieb. et Succ. (Inouye et al., 1977)
and D. schneideriana Rehder (Frederiksen et al., 1999)
3.2.4 Philadelpheae; Kirengeshoma
In the present work we found loganin (1), sweroside (2), 6-β-hydroxysweroside (3)
and demethylalangiside (4).
36 Hydracyanoside D 37 Hydracyanoside F
O
OGlc
COOMe
OH
39 8-Epiloganin
O
OGlc
COOMeHOOC
38 Secoxyloganin
O
O
OGlc
COOMeO
O
OH
OH
OOH
CNH
O
OGlc
O ONC
O
OGlc
ROCOOH
40 R=H; Demethyl- secologanol
O
O
OHOH
OMe
O
OH
OMe
40a Hydrangeside B 40b Methylgrandifloroside
R= R=
OMe
O
OGlc
OHCH
3
OH
41 Deutziol
O
OGlc
OHCH
3
OH
OH
OH
42 Scabrosidol
O
OH
OHCH
3
O
18a Deutziogenin
O
OH
OHCH
3
O
OH
19a Scabrogenin
10
3.2.5 Philadelpheae; Others
The genera Philadelphus, Carpenteria, Whipplea, Fendlerella have all been
investigated for their flavonoid content (Bohm et al, 1985), but apparently not for
iridoids.
3.2.6 Jamesioideae; Jamesia
In the present work, we have isolated the compounds Arbutin (6), picein (7) and
prunasin (8), and no iridoids were present.
3.2.7 Jamesioideae; Fendlera
Apparently, no chemical work has been done on this genus.
3.3 Chemosystematics
The phylogenetic relationships based on the published DNA sequencing results are
shown in Fig. 1. From the above information, it is difficult to deduce much about the
chemical relationships within the Hydrangeaceae, since only six of the seventeen
genera appears to have been investigated properly for their content of iridoid
glycosides. However, some useful taxonomic information about the interfamilial
relationships can be drawn from the published chemical data. Thus, the iridoids in
Deutzia are closely related to those found in Mentzelia (Loasaceae) (Jensen et al.,
1981; El-Naggar et al., 1982) and they share a peculiar biosynthetic route
(Frederiksen et al., 1999) in formation of the 10-decarboxylated compounds (Fig. 3)
so far solely found in these two genera. In addition, the common occurrence of the
iridoid glucoside 6-β-hydroxysweroside (3) in Kirengeshoma and in Gronovia
scandens L. (Loasaceae) (Rodríguez et al., 2002) may be indicative, since 3 is a
compound that has never been reported from other taxa, and futhermore,
hydroxylation of the 6-position of secoiridoids appears to be almost unknown
otherwise. Taken together, this indicate a common ancestry of the two families
Hydrangeaceae and Loasaceae, as it is also found in the DNA sequence investigations
(Fig. 1). On the other hand, many of the simple iridoid glucosides shown in Fig. 2,
namely compounds 1, 11-14 and also 31 and 38 are shared between Hydrangea and
Loasaceae, but these compounds are common in most other families in Dipsacales
and Gentianales.
Hydrangeaceae also share many of the simple compounds above with Cornaceae,
however, the occurrence of the rare esters of loganin (1a and 12a) in Hydrangea
paniculata are particularly interesting since these same compounds are also reported
from Cornaceae, namely 1a from Alangium platanifolium (Sieb. & Zucc.) Harms
(Otsuka et al., 1996) and 5a from A. lamarckii Thwaites (Itoh et al., 2001). Similarly,
the finding of demethylalangiside (4) in Kirengeshoma is paralleled by the occurrence
of this and many similar ipecac alkaloids in Alangium (Itoh et al., 2001). Otherwise,
compounds from this biosynthetic pathway (Fig. 3) is solely found in a few genera of
Rubiaceae.
11
Acknowledgements
The research project is implemented within the framework of the Action «Supporting
Postdoctoral Researchers» of the Operational Program "Education and Lifelong
Learning" and is co-financed by the European Social Fund (ESF) and the Greek State.
We thank the staff of The Botanical Garden of Copenhagen for providing the plant
material and Dr. Larry Hufford, Washington State University for comments.
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17
Fig. 1. Cladogram of Hydrangeaceae based on maximum parsimony analyses of the
combined matK and rbcL data set. Sequences are downloaded from GenBank.
Numbers above branches are bootstrap values.
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