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2 Institute of Systematic Botany, Ludwig Maximilians University, Menzinger Strasse 67, 80638 Munich, Germany; 3 Institute of Pharmacy, Department of Pharmaceutical Biology, Ludwig Maximilians University, Butenandtstrasse 5-13, Haus B, D-81377 Munich, Germany
Received for publication June 15, 1999. Accepted for publication October 19, 1999.
ABSTRACT
A screening for iridoid compounds of 78 of 315 species from all major groups in Gronoviaceae and Loasaceae has been carried out. The results were compared to the systematic concepts in the family and distribution and ecology of the taxa. Iridoids are present in at least some species of all genera screened. Some simple, monomeric compounds (e.g., loganin, sweroside) are found in all major groups of the two families and represent the basic iridoid inventory. Other compounds are restricted to certain taxonomic groups: nine-carbon iridoids (e.g., deutzioside) are restricted to Mentzelia (Loasaceae subfam. Mentzelioideae), hetero-oligomeric iridoids (e.g., tricoloroside methyl ester, acerifolioside) are restricted to two small groups in Loasa (Loasa ser. Macrospermae and ser. Floribundae, Loasaceae subfam. Loasoideae), and oleosides (e.g., 10-hydroxyoleoside dimethyl ester) are restricted to the large genus Caiophora sensu Weigend). The distribution of certain iridoid compounds thus confirms some of the generic limits. Iridoid phytochemistry does not correlate with systematic entities above the generic level nor does it in any way correlate with the morphological evolution of taxa. Conversely, the amount and complexity of iridoid compounds present in taxa correlate positively with the aridity of their habitat and the extent of mammalian herbivore pressure.
Key Words: generic delimitation • Gronoviaceae • herbivory • iridoids • Loasaceae • oleosides • phytochemistry
Recent advances in systematic botany have shown that the distribution of particular plant metabolites is sometimes highly congruent with molecular phylogenies. Typical and well-known examples are found in the Caryophyllales (Hershkovitz and Zimmer, 1997
) and the glucosinolate clade (Capparales s.l.; Rodman et al., 1993, 1998
). Iridoid compounds have also been considered as potentially useful systematic markers (Jensen, 1992
), and their distribution as currently known is largely restricted to a possibly natural group encompassing families such as Dipsacaceae, Ericaceae, Cornaceae, Gentianaceae, Loganiaceae, Verbenaceae, and Rubiaceae. The discovery of iridoids (Bliss, Danielson, and Abramovitch, 1968
; Kooiman, 1974
) in Loasaceae was thus one of the first characters that was in serious conflict with existing classifications: Loasaceae had never been associated with any of these iridoid-containing groups, but were traditionally considered as allies of the Passifloraceae group of families (Passifloraceae, Turneraceae, Malesherbiaceae; Humboldt, Bonpland, and Kunth, 1823; Cronquist, 1981
). The presence of iridoids and other characters such as floral ontogeny (Leins and Winhard, 1973
; Hufford, 1990
) and ovule structure (Takhtajan, 1980
) quickly led to highly divergent views on the affinities of Loasaceae. Thorne (1983)
was among the first to propose a position of Loasaceae/Loasales near the Dipsacales and Cornales, and this view was subsequently confirmed by molecular data (Hempel et al., 1995
; Xiang, Soltis, and Soltis, 1998
). Consequently, the Loasaceae have now been included in the order Cornales in the Asterids, whereas those groups that were formerly considered as allied (i.e., Passifloraceae and Turneraceae) are included in the Rosids (Bremer, Chase, and Stevens [Angiosperm Phylogeny Group], 1998
).
In spite of the weight placed on the phytochemical data in taxonomical literature, the number of taxa for which phytochemical data were available was very small. It has been claimed that the occurrence of specific dimeric iridoids (consisting of one iridoid and one secoiridoid moiety) in Loasa underscores an affinity of the family to the Cornaceae and Dipsacaceae (Nicoletti et al., 1991
), and later attention was drawn to the fact that oleosides of the type found in Caiophora are otherwise only known from Oleaceae (Nicoletti et al., 1996
). Also, Nicoletti et al. (1996)
alleged that the available data indicated some degree of phytochemical differentiation between the subfamilies Mentzelioideae and Loasoideae. There have even been attempts to correlate the oxidation state of iridoids with an evolutionary progression (Kaplan and Gottlieb, 1982
). All these hypotheses were, however, based on a limited database. In the study presented here a large-scale screening of the family for iridoids was undertaken to clarify distribution and evolutionary patterns of iridoid compounds within the family and to re-evaluate the phytochemical affinities discussed in the literature.
The sampling strategy within Loasales was based on a revised classification of Loasaceae/Loasales (Weigend, 1997
). The Loasaceae in the traditional sense (Urban and Gilg, 1900) are now subdivided into two families: Gronoviaceae (Rchb.) Endl. and Loasaceae Juss. An examination of a wide range of characters led to novel concepts about family and generic limits (Table 1). The Gronoviaceae contain only nine species in four genera. These genera are morphologically isolated palaeopolyploids (Poston and Nowicke, 1993; Weigend, 1997
). Loasaceae, on the other hand, now contain a total of ~315 species in two subfamilies, the predominantly South American Loasoideae (~225 spp.) and the predominantly North and Central American Mentzelioideae (~90 spp.). Within Loasales there is clearly a morphological progression. The Gronoviaceae seem to have retained many primitive characters (corolla morphology in Petalonyx, perianth and androecial morphology in Cevallia, trichome morphology in Gronovia, leaf morphology in Fuertesia) in spite of massive anagenesis and appear to be the most basal extant lineage in the order. Within Loasaceae the Mentzelioideae (as currently defined, i.e., including Schismocarpus) are less advanced than the Loasoideae. Phytochemical data had been published mostly from the highly derived groups in the family Loasaceae, amounting to a total of seven genera of Loasaceae-Loasoideae and Loasaceae-Mentzelioideae (Nasa, Schismocarpus, Mentzelia, Loasa, Caiophora, Blumenbachia, and Eucnide). Detailed published data were available for 19 of 315 species of Loasaceae (6%): six of 225 species of subfamily Loasoideae (<3%) and 13 of 90 species of subfamily Mentzelioideae (14%). This study therefore concentrated on the Loasoideae, which are underrepresented in the existing literature.
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MATERIALS AND METHODS
Plant material
All the material was either collected in the wild or from cultivated plants. It was air-dried at ambient temperature. Vouchers of all the plants analyzed are housed at the Munich Herbaria (M, MSB; Table 2).
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TLC (thin layer chromatography) was performed on silica with separation system 2 (EtOH-MeOH-H2O 77:15:8) or separation system 3 (PrOH-toluene-HOAc-H2O 25:20:10:10); detection: UV 254 nm, vis after spraying with vanillin/H2SO4.
Preparation of HPLC and TLC samples
One gram of powdered plant material was extracted with 5 mL MeOH in a water bath. After filtration the volume was refilled to 5.0 mL.
Reference compounds
10-Hydroxyoleoside dimethyl ester (Fig. 1.7), tricoloroside methyl ester (Fig. 3.1), acerifolioside (Fig. 3.2), loasafolioside (Fig. 3.4), asaolaside (Fig. 3.3), secoxyloganin (Fig. 1.4), 8-epi-kingiside (Fig. 1.6), sweroside (Fig. 1.5), and secoxyloganin methyl ester (Fig. 1.3) were isolated and identified as described elsewhere (Müller and Weigend, 1998, 1999
; Müller et al., 1998, 1999
).
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). The loganin and loganic acid references were purchased from Fa. Roth (Karlsruhe, Germany) and Extrasynthese S.A. (Genay, France). Deutzioside was a kind gift of F. Bucar, University of Graz.
RESULTS AND DISCUSSION
A screening of a total of 78 species from both families, all four subfamilies, all tribes, and 15 genera of Loasales unequivocally showed that iridoids are widespread in all groups in Loasales. Together with previously published data 90 taxa have now been screened for idioids, amounting to nearly 29% of the group under investigation. The results are given in Table 3
. At least one representative of all genera screened contained some iridoids. Together with the published data, there are now only two monotypical genera (Chichicaste and Fuertesia) for which no phytochemical data are available. Of the taxa screened only a few species, which are scattered over different genera (e.g., Caiophora, Blumenbachia, and Nasa), lacked detectable amounts of iridoids. Even the most isolated members of Gronoviaceae, the highly divergent genera Gronovia (Gronovioideae) and Petalonyx (Petalonychoideae), contain some monomeric iridoids. Presence of iridoids (e.g., secoxyloganin, 8-epi-kingiside, loganic acid; Fig. 1) is evidently the plesiomorphic condition in Loasales. This confirms the view that Loasaceae/Gronoviaceae belong near other iridoid-containing families, namely the Cornaceae, Hydrangeaceae, and Dipsacaceae.
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In Loasaceae neither subfamily Mentzelioideae nor the more speciose subfamily Loasoideae can be defined by phytochemistry. However, at the generic and infrageneric level the distribution of some iridoids shows clear taxonomic patterns. Jensen, Mikkelsen, and Nielsen's (1981)
assumption that iridoids devoid of carbon 10 (e.g., Fig. 2.1, 2.2) are present only in the genus Mentzelia was corroborated by the detection of several nine-carbon iridoids in additional Mentzelia species by El-Naggar, Beal, and Doskotch (1982)
and Catalano et al. (1992, 1995)
. Our screening also failed to find any nine-carbon iridoids in Gronoviaceae and Loasoideae. Damtoft, Jensen, and Nielsen (1993)
and Rodriguez et al. (1997)
presented data on loganin-related iridoids in the other genera of Mentzelioideae (Eucnide and Schismocarpus), but failed to find the typical nine-carbon iridoids reported from Mentzelia. The subfamily Mentzelioideae can thus not be defined by phytochemistry.
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) are restricted to subfamily Loasoideae, but they are by no means universally present. Dimeric and trimeric iridoids (Fig. 3) of different moieties ("mixed type" = hetero-oligomeric) are now known to be restricted to a small group of species in Loasa ser. Macrospermae and Loasa ser. Floribundae (Müller et al., 1998, 1999
; Müller and Weigend 1998, 1999
), i.e., they are not even universally present in the genus Loasa (sensu Weigend, 1997
), let alone in the subfamily Loasoideae.
Oleosides, initially reported from Caiophora pentlandii (Nicoletti et al., 1996
), have now been shown to be widespread in all sections of Caiophora (sensu Weigend, 1997
; Müller et al., 1999
) and are mainly present as monomers (10-hydroxyoleoside dimethyl ester; Fig. 1.7). They are absent from all other genera screened, including all close allies of Caiophora such as Loasa, Scyphanthus, and Blumenbachia. Oleosides and hetero-oligomeric iridoids are thus restricted to Caiophora and Loasa, respectively. These genera are highly derived in all morphological aspects (Weigend, 1997
) and share a highly specific pollination biology (Schlindwein and Wittmann, 1997
). They are evidently recent groups in the family. All other genera in Loasoideae and especially the more primitive ones (Xylopodia, Presliophytum, Kissenia, Huidobria, and Klaprothia) lack these compounds. A de novo invention of oleosides and oligomeric iridoids in Caiophora and Loasa, respectively, is the only parsimonious explanation for their presence. The presence of oleosides and oligomeric iridoids in Cornaceae/Dipsacaceae and Loasaceae is thus not a common derived character (synapomorphy), but has evolved independently in these groups. It is a case of parallel evolution.
Attempts to correlate the amount, or the complexity, or the oxidation state (Kaplan and Gottlieb, 1982
) of iridoid compounds with evolutionary progress are problematical. Some comparatively primitive branches of Loasaceae (e.g., Kissenia) have a wide range of iridoid compounds, whereas in some of the most highly derived members of Caiophora (e.g., ornithophilic C. buraeavii) no iridoids could be detected. Also, the large and very actively speciating Andean genus Nasa (~100 spp.) with its numerous morphological derivations (Weigend and Rodriguez, 1998
) contains but small amounts of a few iridoids and only of common types (loganin, loganic acid, secoxyloganin and 8-epi-kingiside). Morphological and phytochemical evolution in Loasaceae/Gronoviaceae were not parallel.
Phytochemistry, like most morphological characters, correlates at least as often with habitat and ecology as with phylogenetic progression. A comparison of the iridoid data, morphological characters, and the known distribution of Loasaceae/Gronoviaceae seems to indicate an ecological role of iridoid compounds. All three major groups in Loasaceae that have undergone radiations in dry and/or desertic habitats with high mammalian herbivore pressure (Caiophora, Loasa, and Mentzelia) have undergone considerable phytochemical evolution and contain high levels and/or a wide range of different iridoid compounds. Similarly, Kissenia, growing in areas of southwestern and northeastern Africa, where grazing/browsing by various species of gazelle seriously limits vegetation cover, contains a wide range of different iridoid compounds. The highest level of iridoid compounds (~12% tricoloroside methyl ester) in Loasaceae was encountered in the seeds of deserticolous Loasa ser. Macrospermae, which are the largest seeds anywhere in Loasaceae and contain large amounts of oils and starch, i.e., possibly an extremely attractive food source for rodents. The seeds remain dormant for a long dry season (
10 mo), and seed predation could therefore be a very serious problem. However, both the seeds themselves and the isolated tricoloroside methyl ester are very bitter to the human palate (own experiments). Secoiridoids are known to be bitter (Ghisalberti, 1998
), e.g., amarogentin and gentiopicrin, the bitter principles in gentian roots (Gentianae radix from Gentiana lutea; Pharmacopoea Europaea, 1997). Protection is especially important for the seeds, which are the only part of the plant that are never covered by stinging hairs and/or harsh scabrid trichomes (all the rest of the aboveground part of the plants including the inside of the carpels, the anthers and the petals can be covered with these protective trichomes in Loasaceae). One function of the iridoids in Loasaceae could be to deter herbivores.
Conversely, the large genus Nasa and some of the small genera (Klaprothia and Plakothira) from more mesic habitats, where invertebrate pests are more important than mammalian herbivores, contain few different compounds at low overall levels and have developed no novel chemical structures. The same is true for some species of Caiophora that invaded humid habitats and contain few if any iridoids (C. lateritia and C. buraeavii). Nasa and Klaprothia are heavily attacked by caterpillars of Pyralidae and Geometridae (Lepidoptera), and especially in Nasa the damage done can be very extensive (entire populations can be virtually defoliated by pyralid larvae). Nasa has developed no novel iridoid compounds, but it shows a bewildering array of vastly different leaf shapes, including e.g. peltate, pinnate, trifoliate and pinnatisect leaves (e.g., Weigend, 1997, 1998
), whereas all other groups are conservative with regard to leaf shape. This diversification may have occurred because of a "rare type advantage" in an evolutionary process largely driven by heavy leaf predation in Nasa. The relative scarcity of iridoids in many species of Nasa may even have an adaptive background. Sequestered iridoid glycosides are known to be part of the defense system of caterpillars against predaceous ants (Dyer-Lee and Bowers, 1996
). Therefore, iridoids could play an important role in host plant recognition for the specialized herbivores. Their loss together with the highly varied leaf morphology could serve to make host plant recognition more difficult.
Circumstantial evidence thus indicates that complex iridoid compounds and secoiridoids play a role in the deterrence of mammalian herbivores in dry and desert habitats and represent an additional or alternative defence strategy to the stinging and/or harsh indument (stinging hairs and scabrid and glochidiate trichomes) in Loasaceae. Both strategies are comparatively ineffective against invertebrate herbivores. Both indument and phytochemistry are relatively unimportant in habitats where invertebrate pests are the driving evolutionary force and consequently, species of all groups encountered in these habitats generally have a poorly developed indument and few iridoid compounds at comparatively low concentrations. Completely different adaptative strategies are found in these habitats (herbivore evasion, e.g., via accelerated development and evolution of diverse leaf shapes via rare type advantage), which serve to evade the attack of invertebrate pests.
FOOTNOTES
4 Current address: Lewis B. and Dorothy Cullman Program for Molecular Systematics Studies, The New York Botanical Gardens, 200th St. and Southern Boulevard, Bronx, 10458 New York USA. 
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