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Plant Systematics and Evolution

, Volume 284, Issue 1–2, pp 77–98 | Cite as

Evidence for species differentiation within the Ancistrocladus tectorius complex (Ancistrocladaceae) in Southeast Asia: a molecular approach

  • Harald MeimbergEmail author
  • Heiko Rischer
  • Florian G. Turini
  • Voradol Chamchumroon
  • Michael Dreyer
  • Marcella Sommaro
  • Gerhard Bringmann
  • Günther Heubl
Original Article

Abstract

Representatives of the genus Ancistrocladus, woody lianas of tropical Africa and Asia, contain pharmaceutically interesting alkaloids and have been the subjects of intensive phytochemical investigations. In Southeast Asia, Ancistrocladus tectorius, previously regarded as the only species of the genus from this region, is extremely polymorphic with respect to naphthylisoquinoline alkaloids, indicating that this taxon might be comprised of several morphologically similar species. We performed a comparative study of the ITS region of nuclear rDNA and of the trnK intron of cpDNA as well as an ISSR fingerprint analysis. Using 75 samples of A. tectorius from 21 locations in comparison to samples of other Ancistrocladus species from Asia and from West and Central Africa, we investigated patterns of species differentiation within this taxon. We found the high variability of chemical compounds described for A. tectorius to be paralleled by a high genetic variability of the units that have been assigned to this taxon. Samples assigned to A. tectorius were paraphyletic with respect to species from the Indian subcontinent, and intraspecific variability was comparable to interspecific variability among the African taxa. In addition, groups of individuals occurring in sympatry were found to be more similar to those from other locations, suggesting low levels of gene flow between those sympatric groups. This indicates either a considerable number of hybridization events during the evolution of A. tectorius or the existence of several distinguishable species not yet recognized. Our results are a first step in the development of species or population-specific markers for the prediction of the alkaloid spectrum of samples. This will help to improve the reproducibility of phytochemical research on Ancistrocladus.

Keywords

Ancistrocladus ITS trnK intron ISSR fingerprinting Naphthylisoquinoline alkaloids 

Notes

Acknowledgments

The authors thank R. Pooma and T. Jangonsak (BKF Forest Herbarium, Bangkok) and H.A. Hadi (University of Malaya) for providing valuable plant material and for their help during the excursions in Thailand and Malaysia. Thanks are due to the directors and curators of the herbaria K, KLU, M, MSB, and P for the opportunity to study type specimens and collections. Also gratefully acknowledged are C. Bräuchler for providing plant material from SE Asia and A. Hurrel, Dr. M. Wohlfarth, and Dr. K. Wolf for assistance in the field. Collection took place with permission of the respective authorities. We would especially like to thank Tanja Ernst for the excellent technical assistance in the laboratory and owe many thanks to F. Thiel and A. Kreiner from the Botanical Garden of the University of Würzburg for expertly growing most of the living material of Ancistrocladus. The research presented in this study was supported by grants from the Deutsche Forschungsgemeinschaft (DFG, He 2671/2-3 and Br 699/14-2) and by the Fonds der Chemischen Industrie.

References

  1. Applied Biostatistics (2002) NTSYSpc version 2.10w, 1996-2002Google Scholar
  2. Boyd MR, Hallock YF, Cardellina JH II, Manfredi KP, Blunt JW, McMahon JB, Buckheit RW, Bringmann G, Schäffer M, Cragg GM, Thomas DW, Jato JG (1994) Anti-HIV michellamines from Ancistrocladus korupensis. J Med Chem 37:1740–1745CrossRefPubMedGoogle Scholar
  3. Bringmann G, Kinzinger L (1992) (+)-Ancistrocline, a naphthylisoquinoline alkaloid from Ancistrocladus tectorius. Phytochemistry 31:3297–3299CrossRefGoogle Scholar
  4. Bringmann G, Pokorny F (1995) The naphthylisoquinoline alkaloids. In: Cordell GA (ed) The alkaloids. Academic Press, New York, pp 127–271Google Scholar
  5. Bringmann G, François G, Aké Assi L, Schlauer J (1998) The alkaloids of Triphyophyllum peltatum (Dioncophyllaceae). Chimia 52:18–28Google Scholar
  6. Bringmann G, Wohlfarth M, Rischer H, Schlauer J, Brun R (2002) Extract screening by HPLC coupled to MS–MS, NMR, and CD: a dimeric and three monomeric naphthylisoquinoline alkaloids from Ancistrocladus griffithii. Phytochemistry 61:195–204CrossRefPubMedGoogle Scholar
  7. Bringmann G, Dreyer M, Rischer H, Wolf K, Hadi HA, Brun R, Meimberg H, Heubl G (2004) Ancistrobenomine A, the first naphthylisoquinoline oxygenated at Me-3, and related 5,1′-coupled alkaloids, from the “new” plant species Ancistrocladus benomensis. J Nat Prod 67:2058–2062CrossRefPubMedGoogle Scholar
  8. Bringmann G, Dreyer M, Kopff H, Rischer H, Wohlfarth M, Hadi HA, Brun R, Meimberg H, Heubl G (2005) ent-Dioncophylleine A and related dehydrogenated naphthylisoquinoline alkaloids, the first Asian Dioncophyllaceae-type alkaloids, from the “new” plant species Ancistrocladus benomensis. J Nat Prod 68:686–690CrossRefPubMedGoogle Scholar
  9. Buckler ES, Ippolito A, Holtsford TP (1997) The evolution or ribosomal DNA: divergent paralogues and phylogenetic implications. Genetics 145:821–832PubMedGoogle Scholar
  10. Campbell CS, Wojciechowski MF, Baldwin BG, Alice LA, Donoghue MJ (1997) Persistent nuclear ribosomal DNA sequence polymorphism in the Amelanchier agamic complex (Rosaceae). Mol Biol Evol 14:81–90PubMedGoogle Scholar
  11. Cheek M (2000) A synoptic revision of Ancistrocladus (Ancistrocladaceae) in Africa, with a new species from western Cameroon. Kew Bull 55:871–882CrossRefGoogle Scholar
  12. Cheek M, Frimodt-Moller C, Hoerlyck V (2000) A new submontane species of Ancistrocladus from Tanzania. Kew Bull 55:207–212CrossRefGoogle Scholar
  13. Chen Z, Wang B, Qin K, Zhang B, Su Q, Lin Q (1981) Isolation and identification of the alkaloids from Ancistrocladus tectorius. Yaoxue Xuebao 16:519–522Google Scholar
  14. Côté CA, Peculis BA (2001) Role of the ITS2-proximal stem and evidence for indirect recognition of processing sites in pre-rRNA processing in yeast. Nucleic Acids Res 29:2106–2116CrossRefPubMedGoogle Scholar
  15. Cuénoud P, Savolainen V, Chatrou LW, Powell M, Grayer RJ, Chase MW (2002) Molecular phylogenetics of Caryophyllales based on nuclear 18S rDNA and plastid rbcL, atpB, and matK DNA sequences. Am J Bot 89:132–144CrossRefGoogle Scholar
  16. Farris JS, Källersjö M, Kluge AG, Bult C (1995) Testing significance of incongruence. Cladistics 10:315–319CrossRefGoogle Scholar
  17. Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791CrossRefGoogle Scholar
  18. Forster PF, Sork VL (1997) Population and genetic structure of the West African rain forest liana Ancistrocladus korupensis (Ancistrocladaceae). Am J Bot 84:1078–1091CrossRefGoogle Scholar
  19. François G, Bringmann G, Phillipson JD, Aké Assi L, Dochez D, Rübenacker M, Schneider C, Wéry M, Warhurst DC, Kirby GC (1994) Activity of extracts and naphthylisoquinoline alkaloids from Triphyophyllum peltatum, Ancistrocladus abbreviatus and A. barteri against Plasmodium falciparum and P. berghei in vitro. Ann Trop Med Parasitol 90:115–123Google Scholar
  20. Gereau RE (1997) Typification of names in Ancistrocladus Wallich (Ancistrocladaceae). Novon 7:242–245CrossRefGoogle Scholar
  21. Gupta M, Chyi Y-S, Romero-Severson J, Owen JL (1994) Amplification of DNA markers from evolutionarily diverse genomes using single primers of simple-sequence repeats. Theor Appl Genet 89:998–1006CrossRefGoogle Scholar
  22. Hallock YF, Manfredi KP, Blunt JW, Cardellina JH II, Schaeffer M, Gulden K-P, Bringmann G, Lee AY, Clardy J, François G, Boyd MR (1994) Korupensamines A–D, novel antimalarial alkaloids from Ancistrocladus korupensis. J Org Chem 59:6349–6355CrossRefGoogle Scholar
  23. Hardig TM, Soltis PS, Soltis DE (2000) Diversification of the North American shrub genus Ceanothus (Rhamnaceae): conflicting phylogenies from nuclear ribosomal DNA and chloroplast DNA. Am J Bot 87:108–123CrossRefPubMedGoogle Scholar
  24. Hershkovitz MA, Zimmer EA (1996) Conservation patterns in angiosperm rDNA-ITS2 sequences. Nucleic Acids Res 24:2857–2867CrossRefPubMedGoogle Scholar
  25. Hughes CE, Bailey CD, Harris SA (2002) Divergent and reticulate species relationships in Leucaena (Fabaceae) inferred from multiple data sources: insights into polyploid origins and nrDNA polymorphism. Am J Bot 89:1057–1073CrossRefGoogle Scholar
  26. Johnson LA, Soltis DE (1994) MatK DNA sequences and phylogenetic reconstruction in Saxifragaceae s.str. Syst Bot 19:143–156CrossRefGoogle Scholar
  27. Kress WJ, Wurdack KJ, Zimmer EA, Weigt LA, Janzen DH (2005) Use of DNA barcodes to identify flowering plants. Proc Nat Acad Sci 102(23):8369–8374CrossRefPubMedGoogle Scholar
  28. Lahaye R, van der Bank M, Bogarin D, Warner J, Pupulin F, Gigot G, Maurin O, Duthoit S, Barraclough TG, Savolainen V (2008) DNA barcoding the floras of biodiversity hotspots. Proc Nat Acad Sci 105(8):2923–2928CrossRefPubMedGoogle Scholar
  29. Lipscomb D, Platnick N, Wheeler Q (2003) The intellectual content of taxonomy: a comment on DNA taxonomy. Trends Ecol Evol 18:65–66CrossRefGoogle Scholar
  30. Liu J-S, Schardl CL (1994) A conserved sequence in internal transcribed spacer 1 of plant nuclear rRNA genes. Plant Mol Biol 26:775–778CrossRefPubMedGoogle Scholar
  31. Manfredi KP, Britton M, Vissieche V, Pannell LK (1996) Three new naphthyldihydroisoquinoline alkaloids from Ancistrocladus tectorius. J Nat Prod 59:854–859CrossRefPubMedGoogle Scholar
  32. Mathews DH, Zuker M, Turner DH (2001) RNAstructure version 3.6 (1996–2001)Google Scholar
  33. Meimberg H, Dittrich P, Bringmann G, Schlauer J, Heubl G (2000) Molecular phylogeny of Caryophyllidae s.l. based on matK-sequences with special emphasis on carnivorous taxa. Plant Biol 2:218–228CrossRefGoogle Scholar
  34. Meimberg H, Wistuba A, Dittrich P, Heubl G (2001) Molecular phylogeny of Nepenthaceae based on cladistic analysis of plastid trnK intron sequence data. Plant Biol 3:154–175CrossRefGoogle Scholar
  35. Meimberg H, Thalhammer S, Brachmann A, Heubl G (2006a) Comparative analysis of a translocated copy of the trnK intron in the carnivorous genus Nepenthes (Nepenthaceae). Mol Phyl Evol 39:478–490CrossRefGoogle Scholar
  36. Meimberg H, Abele T, Bräuchler C, McKay JK, Pérez de Paz PL, Heubl G (2006b) Molecular evidence for adaptive radiation of Micromeria Benth. (Lamiaceae) on the Canary Islands as inferred from chloroplast and nuclear DNA sequences and ISSR fingerprint data. Mol Phyl Evol 41:566–578CrossRefGoogle Scholar
  37. Montagnac A, Hadi AH, Remy F, Pais M (1995) Isoquinoline alkaloids from Ancistrocladus tectorius. Phytochemistry 39:701–704CrossRefGoogle Scholar
  38. Nei M, Li WH (1979) Mathematical model for studying genetic variation in terms of restriction endonucleases. Proc Natl Acad Sci USA 76:5269–5273CrossRefPubMedGoogle Scholar
  39. Nguyen AH, Sung TV, Ripperger H, Adam G (1996) Some results from a chemical study on Vietnamese Ancistrocladus cochinchinensis. Tap Chi Hao Hoc 34:89–93Google Scholar
  40. Nguyen AH, Porzel A, Ripperger H, Bringmann G, Schäffer M, God R, Sung TV, Adam G (1997) Naphthylisoquinoline alkaloids from Ancistrocladus cochinchinensis. Phytochemistry 45:1287–1291CrossRefGoogle Scholar
  41. Peculis BA, Greer CL (1998) The structure of the ITS2-proximal stem is required for pre-rRNA processing in yeast. RNA 4:1610–1622CrossRefPubMedGoogle Scholar
  42. Ponte-Sucre A, Gulder T, Wegehaupt A, Albert C, Rikanovic C, Schaeflein L, Frank A, Schultheis M, Unger M, Holzgrabe U, Bringmann G, Moll H (2009) Structure–activity relationship and studies on the molecular mechanism of leishmanicidal N,C-coupled arylisoquinolinium salts. J Med Chem 52:626–636Google Scholar
  43. Rischer H, Heubl G, Meimberg H, Dreyer M, Hadi HA, Bringmann G (2005) Ancistrocladus benomensis (Ancistrocladaceae): a new species from Peninsular Malaysia. Blumea 50:357–365Google Scholar
  44. Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574CrossRefPubMedGoogle Scholar
  45. Ruangrungsi H, Wongpanchi V, Tantivatana P, Cowe HJ, Cox PJ, Funayama S, Cordell GA (1985) Traditional medicinal plants of Thailand, V. Ancistrotectorine, a new naphtaleneisoquinoline alkaloid from Ancistrocladus tectorius. J Nat Prod 48:529–535CrossRefGoogle Scholar
  46. SAS (2007) JMP, version 7. SAS Institute, Cary, NCGoogle Scholar
  47. Schneider S, Kueffer J-M, Roessli D, Excoffier L (2000) Arlequin version 2.000: a software for population genetic analysis. Genetics and Biometry Laboratory, University of Geneva, GenevaGoogle Scholar
  48. Seberg O, Humphries CJ, Knapp S, Stevenson DW, Petersen G, Scharff N, Andersen NM (2003) Shortcuts in systematics? A commentary on DNA-based taxonomy. Trends Ecol Evol 18:63–65CrossRefGoogle Scholar
  49. Simmons MP, Ochoterena H (2000) Gaps as characters in sequence based phylogenetic analyses. Syst Biol 49:369–381CrossRefPubMedGoogle Scholar
  50. Städler T, Delph LF (2002) Ancient mitochondrial haplotypes and evidence for intragenic recombination in a gynodioecious plant. Proc Natl Acad Sci USA 99:11730–11735CrossRefPubMedGoogle Scholar
  51. Swofford DL (2002) PAUP*. Phylogenetic analysis using parsimony (*and other methods). Version 4.0b10. Sinauer Associates, Sunderland, MAGoogle Scholar
  52. Tautz D, Arctander P, Minelli A, Thomas RH, Vogler AP (2002) DNA points the way ahead in taxonomy. Nature 418:479CrossRefPubMedGoogle Scholar
  53. Tautz D, Arctander P, Minelli A, Thomas RH, Vogler AP (2003) A plea for DNA taxonomy. Trends Ecol Evol 18:70–74CrossRefGoogle Scholar
  54. Taylor CM, Gereau RE, Walters GM (2005) Revision of Ancistrocladus Wall. (Ancistrocladaceae). Ann Missouri Bot Gard 92:360–399Google Scholar
  55. Tsitrone A, Kirkpatric M, Levin DA (2003) A model for chloroplast capture. Evolution 57:1776–1782PubMedGoogle Scholar
  56. Van Steenis CGGJ (1948) Flora Malesiana, series I—seed plants, Ancistrocladaceae, vol 4. National Herbarium Nederland, LeidenGoogle Scholar
  57. Wendel JF, Schnabel A, Seelanan T (1995) An unusual ribosomal DNA sequence from Gossypium gossypioides reveals ancient, cryptic, intergenomic introgression. Mol Phyl Evol 4:298–313CrossRefGoogle Scholar
  58. Wolfe AD, Xiang QY, Kephart SR (1998) Diploid hybrid speciation in Penstemon (Scrophulariaceae). Proc Natl Acad Sci USA 95:5112–5115CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  • Harald Meimberg
    • 1
    Email author
  • Heiko Rischer
    • 2
  • Florian G. Turini
    • 3
  • Voradol Chamchumroon
    • 4
  • Michael Dreyer
    • 5
  • Marcella Sommaro
    • 3
  • Gerhard Bringmann
    • 5
  • Günther Heubl
    • 3
  1. 1.CIBIOUniversity of PortoVairãoPortugal
  2. 2.VTT BiotechnologyEspooFinland
  3. 3.Department Biology I, Section: Biodiversity Research-Systematic BotanyLudwig-Maximilians-Universität MünchenMunichGermany
  4. 4.Department of National Parks, Wildlife and Plant ConservationThe Forest Herbarium (BKF)BangkokThailand
  5. 5.Institute of Organic ChemistryJulius-Maximilians-Universität WürzburgWürzburgGermany

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