Molecular Systematics

Angiosperm Taxonomy and Classification

An ordinal classification for the families of flowering plants

Authored by the Angiosperm Phylogeny Group (eds. Kåre Bremer, Mark W. Chase and Peter F. Stevens, in alphabetical order), Annals of the Missouri Botanical Garden 85 (4): 531-553.
Publication date: 31 December 1998.

For the past 264 years, since the publication of Linnaeus' Systema Naturae, botanists have been trying to improve the way in which plants are classified. French botanists, beginning with Adanson in 1763 and Jussieu in 1789, developed what they considered to be "natural systems", as opposed to that of Linnaeus' sexual system, which was admittedly artificial. The meaning of "natural system" continued to evolve, and with the addition of Darwin's concept of evolution it has come to mean something quite different than that of the French botanists. In the last 50 years, taxonomists have based classification on an evolutionary hierarchy, closely related species grouped together, first in genera, and then up to higher levels.

In this century, new categories of data have become available as the basis for classification. Morphology has long been the mainstay of taxonomy, but in the last 40 years new technologies have aided collection of anatomical and phytochemical data. The basic assumption however has remained that traits useful for identifying plants were also the best basis for classification. Recently it has been argued that all data should be integrated; it was not a matter of one category of information versus the others, but rather it was important to combine all data into one system. When DNA sequencing was developed in the mid-1980s, the stage was set for the inclusion of genetic studies (gene sequences). Computers were perfectly suited to these data, and the evaluation of relationships of all families of flowering plants became feasible as technology for sequencing DNA improved.

In 1993, Chase, Soltis, Olmstead and 39 other researchers published the first paper that evaluated the feasibility of analysing 500 DNA sequences from a representative sampling of families. There were several doubts about this process: could the computers and software then available deal with the complexity of such an enormous dataset, did gene sequences in spite of their functional constraints still contain evolutionary information, and would the patterns found with the first gene (the large subunit of RuBisCO, an important photosynthetic gene) be repeated with other genes? This first dataset took approximately 12 years to assemble, and no one was sure how long it would take to produce the next one, this time for a gene with a completely different product. It was clear that a gene with a completely different function should be used. About this time, automated sequencers were developed, allowing a rapid increase in gene sequencing. In 1997, this resulted in the publication by Soltis, Soltis, Nickrent et al. of the second large dataset for 18S nuclear ribosomal DNA, which produced similar patterns. Also in 1997, the results of a third large analysis of a gene, one involved in respiration in chloroplasts, were reported (by Savolainen, Chase, Hoot et al. and this too was highly similar. As important as the similarity of these studies was the fact that combining these data resulted in incredibly clear patterns of relationships. In 1998, the first large phylogenetic analysis of morphological, anatomical and phytochemical data was published by Nandi, Chase and Endress, and this too gave highly similar patterns.

All these analyses pointed in a single direction. All taxonomists, regardless of whether they worked on morphology or DNA, could now participate in the process of classification. More importantly, classification could now become predictive and refutable because it was based on data that were clearly visible to all researchers. If predictions failed, then the reasons should be sought and the classification improved. The new classification is thus both a tool for focusing research and a product of that research.

The new system of classification provides some wonderful examples of plants that previous taxonomists completely misunderstood, but it also demonstrates that large numbers of families were well understood. It is not a complete negation of all previous botanical research as some articles in the popular press have stated, neither does it overthrow the system of botanical nomenclature that began with Linnaeus nor refute Darwin. Quite the opposite, it draws upon a long history of debate and changing ideas about how the process of classification should be carried out. The new classification is constructed on the same lines of evidence and procedures that botanists have always used, but significantly in recent years this evidence has been augmented with massive amounts of genetic data, so that for the first time evolutionary patterns can be discerned clearly.

Some would assume that all these DNA data obviate the need for other kinds of study, but this is exactly the wrong conclusion. It makes the need for extension of all kinds of botanical study even more important because it is only through the improved knowledge of all types of data that predictivity can be enhanced. If classification were an end point in itself, then perhaps we could eliminate all other forms of botanical research except genetic studies, but classification is not an end at all. It is only the first step, and the really exciting prospects are those that we face now as we make use of the first predictive system of classification for any major group of organisms. Although the new system does not "turn the botanical world on its head" as one reporter recently wrote, it does represent a watershed in the way in which classifications are constructed. As another article in the popular press accurately reported, "a rose is still a rose, but everything else has indeed changed".

Other relevant papers:

Chase, M. W., D. Soltis, R. G. Olmstead, D. Morgan, D. H. Les, B. Mishler, M. R. Duvall, R. A. Price, H. G. Hills, Y-L. Qiu, K. A. Kron, J. H. Rettig, E. Conti, J. D. Palmer, J. R. Manhart, K. J. Sytsma, H. J. Michaels, W. J. Kress, K. G. Karol, W. D. Clark, M. Hedrén, B. S. Gaut, R. K. Jansen, K-J. Kim, C. F. Wimpee, J. F. Smith, G. R. Furnier, S. H. Straus, Q-Y. Xiang, G. M. Plunkett, P. S. Soltis, S. M. Swensen, S. E. Williams, P. A. Gadek, C. J. Quinn, L. Eguiarte, E. Golenberg, G. H. Learn, S. W. Graham, S. C. H. Barrett, S. Dayanandan, and V. A. Albert. 1993. Phylogenetics of seed plants: an analysis of nucleotide sequences from the plastid gene rbcL. Annals of the Missouri Botanical Garden 80: 528-580.
Soltis, D. E., P. S. Soltis, D. L. Nickrent, L. A. Johnson, W. J. Hahn, S. B. Hoot, J. A. Sweere, R. K. Kuzoff, K. A. Kron, M. W. Chase, S. M. Swensen, E. A. Zimmer, S.-M. Chaw, L. J. Gillespie, W. J. Kress, and K. J. Sytsma. 1997. Angiosperm phylogeny inferred from 18S ribosomal DNA sequences. Annals of the Missouri Botanical Garden 84: 1-49.
Soltis, D. E., C. Hibsch-Jetter, P. S. Soltis, M. W. Chase, and J. S. Farris. 1997. Molecular phylogenetic relationships among angiosperms: an overview based on rbcL and 18S rDNA sequences. Pp. 157-178 in K. Iwatsuki and P. H. Raven (eds.), Evolution and Diversification of Land Plants, Springer -Verlag, Tokyo.
Soltis, D. E., P. S. Soltis, M. Mort, M. W. Chase, V. Savolainen, S. B. Hoot, and C. M. Morton. 1998. Inferring complex phylogenies using parsimony: an empirical approach using three large DNA data sets for angiosperms. Systematic Biology 47: 32-42.
Nandi, O., M. W. Chase, and P. K. Endress. 1998. A combined cladistic analysis of angiosperms using rbc L and non-molecular data sets. Annals of the Missouri Botanical Garden 85: 137-212.
Chase, M. W. and A. V. Cox. 1998. Gene sequences, collaboration, and analysis of large data sets. Australian Systematic Botany11: 215-229.
Chase, M. W. and V. A. Albert. 1998. A perspective on the contribution of plastid rbcL DNA sequences to angiosperm phylogenetics. Pp. 488-507, in Soltis, Soltis, and Doyle [eds.], Molecular Systematics of Plants II: DNA sequencing. Kluwer Academic Publishers, Boston.
Källersjö, M., J. S. Farris, M. W. Chase, B. Bremer, M. F. Fay, and K. Bremer. 1999. Simultaneous parsimony jackknife analysis of 2538 rbcL DNA sequences reveals support for major clades of green plants, land plants, seed plants, and flowering plants. Plant Systematics and Evolution: in press.
Savolainen, V., M. W. Chase, S. B. Hoot, C. M. Morton, D. E. Soltis, C. Bayer, M. F. Fay, A. Y. de Bruijn, S. Sullivan, and Y.-L. Qiu. Phylogenetics of flowering plants based upon a combined analysis of plastid atpB and rbcL gene sequences, submitted to Systematic Biology on 28 Oct 1998.

The new classification list with cladogram is available as a web page or Microsoft Word format.