Ancistrocladaceae and Dioncophyllaceae: Botanically Exciting and Phytochemically Productive Tropical Lianas

1. Key Words:

Palaeotropical plants; Caryophyllidae; Nepenthales; Ancistrocladaceae and Dioncophyllaceae (see also 'Naphthylisoquinoline Alkaloids'); Ancistrocladus, Triphyophyllum; Dioncophyllum; Habropetalum; botanical and morphological characteristics; carnivory; cultivation of plants in the greenhouse (in collaboration with the Botanical Garden of the University of Würzburg); chemotaxonomy; molecular phylogeny and systematic position (in collaboration with Prof. G. Heubl, Institut für Systematische Botanik der LMU München); production of plant cell cultures.

2. Graphical Abstract:

Subtopic A:

Molecular Phylogeny of Dioncophyllaceae and Ancistrocladaceae within the Nepenthales with Particular Focus on the Carnivorous Taxa Nepenthaceae, Drosophyllaceae, and Droseraceae

Figure 1: Cladogram summarizing the phylogenetic relationships of the naphthylisoquinoline alkaloids producing palaeotropical plant families Dioncophyllaceae and Ancistrocladaceae among the taxa of Caryophyllidae s.1. Morphological peculiarities of some representatives of the Dioncophyllaceae and Ancistrocladaceae and related plant families are presented in the pictures given above: (a) Plumbago indica (Plumbaginaceae) flowering; (b) sundew – the adhesive ‘snap trap’ of Drosera rotundifolia (Droseraceae); (c) the mucilage-secreting glands (= adhesive traps) of Drosophyllum lusitanicum (Drosophyllaceae); (d) pitchers of Nepenthes danseri (Nepenthaceae); (e) carnivorous specimen of Triphyophyllum peltatum (Dioncophyllaceae) with glandular leaves as the insect-trapping organ; (f) T. peltatum fruiting: almost ripe seeds on open fruits with their wings dried up – the only seeds in the plant kingdom that are larger than the fruits from which they stem; (g) characteristic hooked branches of Ancistrocladus species, here from the Cameroonian plant Ancistrocladus korupensis; (h) the Indian liana Ancistrocladus heyneanus developing ripe fruits representing a nut with five irregularly formed 'wings', derived from enlarged sepals. – [Photos: (a-d, f) – H. Rischer; e – H. Huet; g – M. Dreyer; h – B. Wiesen]

Subtopic B:

Dioncophyllaceae and Ancistrocladaceae (Botanical Characteristics)

Figure 2: The Westafrican liana Triphyophyllum peltatum Airy Shaw (Dioncophyllaceae) grown in the greenhouse of the Botanical Garden (Würzburg) – the name Triphyophyllum means ‘three kinds of leaves’, which characterizes this particular genus: (a) a juvenile plant with a rosette of ca. 10 lanceolate leaves; (b) a carnivorous leaf with glandular emergences, which secrete a sticky mucilage and capture invertebrates; (c) a hooked adult leaf specifically formed on elongated shoots, which helps the plant to climb into the canopy of high trees. – [Photos: a – A. Irmer; b – H. Huet; c – H. Rischer]

Figure 3: Triphyophyllum peltatum flowering for the first time (in June 1999) and showing fruit ripening in the greenhouse of the Botanical Garden of the University of Würzburg: (a) T. peltatum flowering: the flowers open in the morning and start withering in the evening of the very same day; (b) fruit ripening: the ovary enlarged into an obovoid capsule within 10 days after anthesis; (c-d) opening young fruit with developing seeds showing a rapid growth of the circular wing surrounding the embryo and the funicle; (e) almost ripe seeds on open fruits with their wings dried up – finally, the wing reached a diameter of 10 cm with the embryo embedded in a disk of endosperm positioned in the center; (f) ripe seeds. – [Photos: H. Rischer]

Figure 4: Ancistrocladus benomensis Rischer & G. Bringmann, a new species, discovered in 1999 from an isolated mountain of Peninsular Malaysia, and flowering for the the first time (in March 2004) in the greenhouse of the Botanical Garden of the University of Würzburg: (a) a young plant of A. benomenis cultivated in the greenhouse; (b,c) a lateral branch with rosette leaves and inflorescences; (d-f) flowers in buds; (d) young flowers with view on reflexed sepals and petals, and (f) flower with five spots on the inner surface of the petals. – [Photos: M. Dreyer]

3. Brief Description:

The systematic position of the palaeotropical plant families Ancistrocladaceae and Dioncophyllaceae [1] indigenous to the tropical rain forests of Africa and Southeast Asia, was unclear for a long time. Comparison of DNA sequence data [2,3] have now permitted a reliable placement within the Caryophyllidae sensu lato as a sister clade of the carnivorous Drosophyllaceae, in close vicinity to the likewise carnivorous Nepenthaceae and Droseraceae, along with a second closely related clade combining the Plumbaginaceae, Polygonaceae, Tamaricaceae, and Frankeniaceae (see Figure 1).
Triphyophyllum, a monotypic genus within the Dioncophyllaceae, is also known to produce carnivorous glandular leaves during a certain period of life [4-7]. The name Triphyophyllum is derived from the three different kinds of leaves that this plant can form (see Figure 2): (a) lanceolate juvenile leaves, (b) carnivorous glandular leaves, and (c) hooked adult leaves. In the greenhouse of the Botanical Garden of the University of Würzburg, we have been the first to grow Triphyophyllum peltatum (Hutch. & Dalz.) Airy Shaw to maturity, and have observed its life cycle under controlled conditions until flowering and development of its characteristic ‘gymnosperm’ fruits (see Figure 3) [7]. Besides this rare and difficult-to-cultivate liana, only two other species, Dioncophyllum thollonii Baillon and Habropetalum dawei (Hutch. & Dalz.) Airy Shaw, belong to the small Dioncophyllaceae family.
The related, yet non-carnivorous, monotypic genus Ancistrocladus Wall. (Ancistrocladaceae) comprises about 20 species, and is characterized by a disjunct distribution in the palaeotropics with two areas of speciation, one in tropical West, Central, and East Africa, and one in South East Asia. All taxa are scandent shrubs or woody lianas with tendril-like modified shoots provided with typical circinate woody hooks as climbing devices (see Figure 1g). In the Botanical Garden of Würzburg, currently specimens of more than 12 Ancistrocladaceae species are being cultivated, among them Ancistrocladus heyneanus from India [8], A. cochinchinensis from Vietnam, A. abbreviatus from Ghana [8,9], and also some probably new Ancistrocladus species from the Congo basin [10,11]. In 1999, we discovered a phytochemically unusual Ancistrocladus species (see Figure 4a) from an isolated mountain of Peninsular Malaysia, which is morphologically, phytochemically, and genetically distinguishable from all other South East Asian species. Based on complete material including all stages of flowering (see Figure 4b-f) and fruits, and in a close cooperation with G. Heubl et al. (LMU München) we provided a botanical description of this new Ancistrocladus species. According to its site of discovery, we named it Ancistrocladus benomensis [12].
Both plant families, the Ancistrocladaceae and the Dioncophyllaceae, have in common that they are the only known ‘producers’ of the naphthylisoquinoline alkaloids, structurally, biosynthetically, and pharmaceutically unique natural biaryl products (see also ‘Naphthylisoquinoline Alkaloids’).

4. Selected Publications

[1]	The Families and Genera of Vascular Plants. V. Flowering Plants – Dicotyledons, Malvales, Capparales and Non-betalain Caryophyllales, Vol. 5 (K. Kubitzki, C. Bayer, eds.), Springer, Heidelberg, 2002. – S. Porembski; Ancistrocladaceae, pp. 25-27. – S. Porembski, W. Barthlott; Dioncophyllaceae, pp. 178-181.
[2]	H. Meimberg, P. Dittrich, G. Bringmann, J. Schlauer, G. Heubl; Molecular phylogeny of Caryophyllidae s.1. based on matK sequences with special emphasis on carnivorous taxa. Plant Biol. 2000, 2, 218-228.
[3]	G. Heubl, G. Bringmann, H. Meimberg; Molecular phylogeny and character evolution of carnivorous plant families in Caryophyllales – revisited. Plant Biol. 2006, 8, 821-830.
[4]	G. Bringmann, J. Schlauer, K. Wolf, H. Rischer, U. Buschbom, A. Kreiner, F. Thiele, M. Duschek, L. Aké Assi; Cultivation of Triphyophyllum peltatum (Dioncophyllaceae), the part-time carnivorous plant. Carniv. Plant Newslett. 1999, 28, 7-13.
[5]	G. Bringmann, M. Wenzel, H. Bringmann, J. Schlauer, L. Aké Assi, F. Haas; Uptake of the amino acid alanine by digestive leaves: proof of carnivory of the tropical liana Triphyophyllum peltatum (Dioncophyllaceae). Carniv. Plant Newslett. 2001, 30, 15-21.
[6]	G. Bringmann, H. Rischer; In vitro propagation of the alkaloid-producing rare African liana, Triphyophyllum peltatum (Dioncophyllaceae). Plant Cell Rep. 2001, 20, 591-595.
[7]	G. Bringmann, H. Rischer, J. Schlauer, K. Wolf, A. Kreiner, M. Duschek, L. Aké Assi; The tropical liana Triphyophyllum peltatum (Dioncophyllaceae): formation of carnivorous organs is only a facultative prerequisite for shoot elongation. Carniv. Plant Newslett. 2002, 31, 44-52.
[8]	G. Bringmann, D. Feineis; Stress-related polyketide metabolism of Dioncophyllaceae and Ancistrocladaceae. J. Exp. Bot. 2001, 52, 2015-2022.
[9]	G. Bringmann, H. Rischer, J. Schlauer, L. Aké Assi; In vitro propagation of Ancistrocladus abbreviatus Airy Shaw (Ancistrocladaceae). Plant Cell Tiss. Org. Cult. 1999, 57, 71-73.
[10]	M. Unger, M. Dreyer, S. Specker, S. Laug, M. Pelzing, C. Neusüß, U. Holzgrabe, G. Bringmann; Analytical characterisation of crude extracts from an African Ancistrocladus species using high-performance liquid chromatography and capillary electrophoresis coupled to ion trap mass spectrometry. Phytochem. Anal. 2004, 15, 21-26.
[11]	G. Bringmann, I. Kajahn, M. Reichert, S.E.H. Pedersen, J.H. Faber, T. Gulder, R. Brun, S.B. Christensen, A. Ponte-Sucre, H. Moll, G. Heubl, V. Mudogo; Ancistrocladinium A and B, the first N,C-coupled naphthyldihydroisoquinoline alkaloids, from a Congolese Ancistrocladus species. J. Org. Chem. 2006, 71, 9348-9356.
[12]	H. Rischer, G. Heubl, H. Meimberg, M. Dreyer, H.A. Hadi, G. Bringmann; Ancistrocladus benomensis (Ancistrocladaceae): a new species from Peninsular Malaysia. Blumea 2005, 50, 357-365.

5. Cooperations and Research Grants:

Plant collection in collaboration with numerous chemists and biologists from tropical countries, among them:

	Prof. Dr. L. Aké Assi (Centre National de Floristique, Abidjan, Ivory Coast);
	Prof. Dr. V. Mudogo (Université de Kinshasha, Republic of Congo);
	Prof. Dr. W. Barthlott (Nees-Institut für Biodiversität der Pflanzen, Universität Bonn);
	Dr. H. Huet (Bio-Oz Biotechnologies Ltd., Israel);
	Dr. R. Haller, Dr. S. Bär (Baobab Farm Ltd., Mombasa, Kenya);
	Prof. Dr. B. Alo (Department of Chemistry, University of Lagos, Nigeria);
	Dr. A.M. Louis (Herbier National de Gabon, Libreville, Gabon);
	Prof. Dr. F.S.K. Tayman (Chemistry Department, University of Cape Coast, Ghana);
	Prof. Dr. A.H.A. Hadi (University of Malaya, Kuala Lumpur, Malaysia);
	Prof. Dr. A. Wickramasinghe (Chemistry Department, University of Peradeniya, Sri Lanka);
	Prof. Dr. A.S. Sankara Narayanan (Sidha and Ayurveda Hospital, Coimbatore, India).

Work on the molecular phylogeny, chemotaxonomy, and systematic position of Dioncophyllaceae and Ancistrocladaceae with Prof. Dr. G. Heubl (Institut für Systematische Botanik der LMU München), sponsored by the Deutsche Forschungsgemeinschaft (DFG) ("Molecular Phylogeny and Chemotaxonomie of the Ancistrocladaceae Plant Family", Individual Grants Br699/7 and Br 699/14-2);

Work on the biosynthetic origin of naphthylisoquinoline alkaloids from Dioncophyllaceae and Ancistrocladaceae plants within a special research project entitled "Biosynthesis of Axially Chiral Alkaloids from Plants" incorporated into the DFG priority programme 1152 "Evolution of Metabolic Diversity", Individual Grant Br 699/9).