Skip to main content
Log in

Molecular phylogeny of Old WorldTrifolium (Fabaceae), based on plastid and nuclear markers

  • Published:
Plant Systematics and Evolution Aims and scope Submit manuscript

Abstract

Phylogenies of Old WorldTrifolium species were constructed using nucleotide sequence data of the internal transcribed spacers (ITS) of nuclear ribosomal DNA and chloroplast DNA restriction site data from PCR-amplified genes and genic regions (rbcL,trnK, andrpoC1–C2). Biogeography, morphological evolution, and the existing classification forTrifolium were examined. The genusTrifolium is strongly supported as monophyletic, however, only one small section (Chronosemium) is monophyletic, although the data are in conflict regarding its placement. The two largest sections of the genus, Sects.Lotoidea andTrifolium, are not supported as monophyletic, as currently circumscribed. Many members of Sect.Lotoidea are basal within the genus, supporting previously-proposed hypotheses concerning plesiomorphic morphological characters and a Mediterranean-Mideast biogeographic origin of the genus.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Badr A. (1995) Electrophoretic studies of seed proteins in relation to chromosomal criteria and the relationships of some taxa ofTrifolium. Taxon 44: 183–191.

    Google Scholar 

  • Baldwin B. G., Sanderson M. J., Porter J. M., Wojciechowski M. F., Campbell C. S., Donoghue M. J. (1995) The ITS region of nuclear ribosomal DNA: a valuable source of evidence of angiosperm phylogeny. Ann. Missouri Bot. Gard. 82: 247–277.

    Google Scholar 

  • Bobrov E. G. (1967) On the span of the genusTrifolium s.l. Bot. Zurn., S.S.R. 52: 1593–1599 (Russian with English summary).

    Google Scholar 

  • Boissier E. (1872)Trifolium. In: Flora Orientalis, 2. Geneva and Basel, pp. 110–156.

  • Britten E. J. (1963) Chromosome numbers in the genusTrifolium. Cytologia 28: 428–449.

    Google Scholar 

  • Bullitta S., Hayward M. D. (1996) Application of RAPD markers to a study of species relationships in the genusTrifolium. In: Pickersgill B., Lock J. M. (eds.) Advances in Legume Systematics, Part 8: Legumes of Economic Importance. Royal Botanic Gardens, Kew, pp. 127–135.

    Google Scholar 

  • Celakovsky L. (1874) Über den Aufbau der GattungTrifolium Österr. Bot Z. 24: 37–45, 75–82.

    Google Scholar 

  • Dowling T. E., Moritz C., Palmer J. D. (1990) Nucleic acids II: Restriction site analysis. In: Hillis D. M., Moritz C., (eds.) Molecular Systematics. Sinauer Associates, Sunderland, pp. 250–317.

    Google Scholar 

  • Downie S. R., Katz-Downie D. S., Rogers E. J., Zujewski H. L., Small E. (1998) Multiple independent losses of the plastidrpoC1 intron inMedicago (Fabaceae) as inferred from phylogenetic analyses of nuclear ribosomal DNA internal transcribed spacer sequences. Canad. J. Bot. 76: 791–803.

    Google Scholar 

  • Doyle J. J. (1995) DNA data and legume phylogeny: a progress report. In: Crisp M., Doyle J. J. (eds.) Advances in Legume Systematics, Part 7: Phylogeny. Royal Botanic Gardens, Kew, pp. 11–30.

    Google Scholar 

  • Doyle J. J., Doyle J. L. (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem. Bull. 19: 11–15.

    Google Scholar 

  • El-Kholy M. A. (1990) Cytology of someTrifolium species. Ph.D. Thesis, unpubl. Al-Azhar University, Cairo.

    Google Scholar 

  • Farris J. S., Källersjo M., Kluge A. G., Bult C. (1995) Testing significance of congruence. Cladistics 10: 315–320.

    Google Scholar 

  • Felsenstein J. (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39: 783–791.

    Google Scholar 

  • Gillett J. M. (1952) The genusTrifolium in southern Arabia and in Africa south of the Sahara. Kew Bulletin, Royal Botanic Gardens, Kew 7: 367–404.

    Google Scholar 

  • Gillett J. M. (1985) Taxonomy and morphology. Clover Science and Technology, Agronomy Monograph 25: 7–69.

    Google Scholar 

  • Hendrych R. (1978) Ein Versuch, die Arealentwicklung der GattungChrysapsis zu erläutern. Preslia 50: 119–137.

    Google Scholar 

  • Heyn C. C. (1981) Trifolieae. In: Polhill R. M., Raven P. H. (eds.) Advances in Legume Systematics, Part 1: Royal Botanic Gardens, Kew, pp. 383–385.

    Google Scholar 

  • Higgins D. G., Bleasby A. J., Fuchs R. (1992) Clustal V: Improved software for multiple sequence alignment. Comp. Appl. Biosciences 8: 189–191.

    Google Scholar 

  • Hossain M. (1961) A revision ofTrifolium in the Nearer East. Notes from Royal Botanic Garden Edinburgh, Aberdeen University Press 23: 387–481.

    Google Scholar 

  • Hu J.-M., Lavin M., Wojciechowski M., Sanderson M. (1999) Phylogenetic systematics of the tribe Millettieae (Leguminosae) based ontrnK/matK sequences and its implications for evolutionary patterns in Papilionoideae. Amer. J. Bot. 87: 418–430.

    Google Scholar 

  • Johnson L. A., Soltis D. E. (1994)matK DNA sequences and phylogenetic reconstruction in Saxifragaceaes. str. Syst. Bot. 19: 143–156.

    Google Scholar 

  • Koch C. (1835)Trifolium. In: Synopsis Florae Germanicae et Helvetica, Vol. 1. Wilmans, Francofurtis and Moenum, pp. 167–176.

  • Kozuharov S. I., Petrova A. V., Markova T. A. (1975) In: Lîve A. (ed.) IOPB chromosome number reports XLVII. Taxon 24: 145–146.

    Google Scholar 

  • Lavin M., Doyle J. J., Palmer J. D. (1990) Evolutionary significance of the loss of the chloroplast-DNA inverted repeat in the Leguminosae. Evolution 44: 390–402.

    Google Scholar 

  • Liston A. (1992) Variation in the chloroplast genesrpoC1 andrpoC2 of the genusAstragalus (Fabaceae): evidence from restriction site mapping of a PCR-amplified fragment. Amer. J. Bot. 79: 953–961.

    Google Scholar 

  • Liston A., Wheeler J. A. (1994) The phylogenetic position of the genusAstragalus (Fabaceae): evidence from the chloroplast genesrpoC1 andrpoC2. Biochem. Syst. Ecol. 22: 377–388.

    Google Scholar 

  • Milligan B. G. (1991) Chloroplast DNA diversity within and among populations ofTrifolium pratense. Curr. Genet. 19: 411–416.

    Google Scholar 

  • Milligan B. G., Hampton J. N., Palmer J. D. (1989) Dispersed repeats and structural reorganization in subclover chloroplast DNA. Mol. Biol. Evol. 6: 355–368.

    Google Scholar 

  • Norris D. O. (1956) Legumes and Rhizobium Symbiosis. Emp. J. Exp.

  • Olmstead R. G., Palmer J. D. (1994) Chloroplast DNA systematics: a review of methods and data analysis. Amer. J. Bot. 81: 1205–1224.

    Google Scholar 

  • Polhill R. M. (1981) Papilionoideae. In: Polhill R. M., Raven P. H. (eds.) Advances in Legume Systematics, Part 1. Royal Botanic Gardens, Kew, pp. 191–208.

    Google Scholar 

  • Pritchard A. J. (1962) Number and morphology of chromosomes in African species in the genusTrifolium L. Australian J. Agric. Res. 13: 1023–1029.

    Google Scholar 

  • Raven P. H., Polhill R. M. (1981) Biogeography of the Leguminosae. In: Polhill R. M., Raven P.H. (eds.) Advances in Legume Systematics, Part 1. Royal Botanic Gardens, Kew, pp. 27–34.

    Google Scholar 

  • Rieseberg L. H., Hanson M. A., Philbrick C. T. (1992) Androdioecy is derived from dioecy in Datiscaceae: evidence from restriction site mapping of PCR-amplified chloroplast DNA fragments. Syst. Bot. 17: 324–336.

    Google Scholar 

  • Saghai-Maroof M. A., Soliman K. M., Jorgensen R. A., Allard R. W. (1984) Ribosomal DNA spacer length polymorphism in barley: Mendelian inheritance, chromosomal location and population dynamics. Proc. Natl. Acad. Sci. USA 81: 8014–8018.

    Google Scholar 

  • Sanderson M. J., Liston A. (1995) Molecular phylogenetic systematics of Galegeae, with special reference toAstragalus. In: Crisp M., Doyle J. J. (eds.) Advances in Legume Systematics, Part 7: Phylogeny. Royal Botanic Gardens, Kew, pp. 331–350.

    Google Scholar 

  • Sanderson M. J., Liston A., Wojciechowski M. F. (1996) Diversification rates in a temperate legume clade: are there “so many species” ofAstragalus (Fabaceae)? Amer. J. Bot. 83: 1488–1502.

    Google Scholar 

  • Sanger F., Nicklen S., Coulson A. R. (1977) DNA sequencing with chain-terminating inhibitors. Proc. Natl. Acad. Sci., USA 74: 5463–5467.

    Google Scholar 

  • Senn H. A. (1938) Chromosome number relation-ships in the Leguminosae. Biblio. Genetica 12: 175–336.

    Google Scholar 

  • Small E. (1989) The evolution of genera in the Leguminosae. In: Stirton C. H., Zarucchi J. L. (eds.) Advances in Legume Biology. Monographs in Systematic Botany, from the Missouri Botanical Garden 29: 467–486.

    Google Scholar 

  • Steele K. P., Udpa B., Chinn D., Curameng O., Throckmorton D., Wojciechowski M. F. (1999) [abstract] Phylogenetic relationships of Tribes Trifolieae and Viceae (Fabaceae). XVI International Botanical Congress, St. Louis, Missouri, USA p. 390.

    Google Scholar 

  • Steele K. P., Udpa B., Chinn D., Curameng O., Throckmorton D., Wojciechowski M. F., Watson L. E., Liston A., Sayed-Ahmed H., Downie S. R., Wojciechowski M. F. (1998) [abstract] Molecular systematics of the Trifolieae: phylogenetic analyses of nuclear and chloroplast DNA sequences. XVTrifolium Conference, Madison, Wisconsin, USA.

  • Steiner J. J., Robinson W. A, Liston A., Taylor N. L. (1997) ITS and RAPD phylogenetic hypotheses and the ecological distributions of North AmericanTrifolium L. (Fabaceae). Amer. J. Bot. 84 [Suppl.]: 235–236.

    Google Scholar 

  • Swofford D. L. (1993) PAUP: Phylogenetic Analysis Using Parsimony, Version 3.1.1. Smithsonian Institution, Washington, DC.

    Google Scholar 

  • Swofford D. L. (1999) PAUP*. Phylogenetic Analysis Using Parsimony (* and Other Methods), Version 4. Sinauer Associates, Sunderland.

    Google Scholar 

  • Taylor N. L. (1985) Clovers around the world. Clover Science and Technology, Agronomy Monograph 25: 1–6.

    Google Scholar 

  • Wexelsen H. (1928) Chromosome numbers and morphology inTrifolium. University of California Publications in Agricultural Sciences 2: 355–376.

    Google Scholar 

  • White T. J., Birns T., Lee S., Taylor J. (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis M., Gelfand D., Sninsky J., White T. (eds.) PCR protocols: A guide to methods and applications. Academic Press, San Diego, pp. 315–322.

    Google Scholar 

  • Winberg G., Hammarskjöld M.-L. (1980) Isolation of DNA from agarose gels using DEAE-paper. Application to restriction site mapping of adenovirus type 16 DNA. Nucleic Acids Res. 8: 253–264.

    Google Scholar 

  • Wojciechowski M. F., Sanderson M. J., Baldwin B. G., Donoghue M. J. (1993) Monophyly of aneuploidAstragalus (Fabaceae): evidence from nuclear ribosomal DNA internal transcribed spacer sequences. Amer. J. Bot. 80: 711–722.

    Google Scholar 

  • Wolfe A. D., Elisens W. J., Watson L. E., dePamphilis C. W. (1997) Using restriction site variation of PCR-amplified cpDNA genes for phylogenetic analysis of Tribe Cheloneae (Scrophulariaceae). Amer. J. Bot. 84: 555–564.

    Google Scholar 

  • Wolfe K. H. (1991) Protein-coding genes in chloroplast DNA: Compilation of nucleotide sequences, database entries and rates of molecular evolution. In: Bogorad L., Vasil I. K. (eds.) The photosynthetic apparatus: molecular biology and operation, Vol. 7B, Cell culture and somatic cell genetics in plants. Academic Press, New York, pp. 467–482.

    Google Scholar 

  • Yokota Y., Kawata T., Iida Y., Kato A., Tanifuji S. (1989) Nucleotide sequences of the 5.8S rRNA gene and internal transcribed spacer regions in carrot and broad bean ribosomal DNA. J. Mol. Evol. 29: 294–301.

    Google Scholar 

  • Zohary M. (1972) Origins and evolution in the genusTrifolium. Bot. Notiser. 125: 501–511.

    Google Scholar 

  • Zohary M., Heller D. (1984) The genusTrifolium. The Israel Academy of Science, Jerusalem.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Watson, L.E., Sayed-Ahmed, H. & Badr, A. Molecular phylogeny of Old WorldTrifolium (Fabaceae), based on plastid and nuclear markers. Pl Syst Evol 224, 153–171 (2000). https://doi.org/10.1007/BF00986340

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00986340

Key words

Navigation