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The Plant Tree of Life: an Overview and Some Points of View1 American Journal of Botany 91(10): 1437±1445. 2004. THE PLANT TREE OF LIFE: AN OVERVIEW AND SOME POINTS OF VIEW1 JEFFREY D. PALMER,2,5 DOUGLAS E. SOLTIS,3 AND MARK W. C HASE4 2Department of Biology, Indiana University, Bloomington, Indiana 47405-3700 USA; 3Department of Botany and the Genetics Institute, University of Florida, Gainesville, Florida 32611 USA; and 4Molecular Systematics Section, Jodrell Laboratory, Royal Botanic Gardens, Kew, Richmond, TW9 3DS, United Kingdom We provide a brief overview of this special issue on the plant tree of life, describing its history and the general nature of its articles. We then present our estimate for the overall topology and, for land plants, divergence times of the plant tree of life. We discuss several major controversies and unsolved problems in resolving portions of this tree. We conclude with a few thoughts about the prospects for obtaining a comprehensive, robustly resolved, and accurately dated plant tree of life and the importance of such a grand endeavor. Key words: algae; endosymbiosis; Gnepines hypothesis; land plants; phylogeny; plastids. To mark the 90th anniversary of this journal, Scott Russell, eukaryotic phylogeny and plastid primary and secondary sym- the then-Immediate Past President of the Botanical Society of biosis. Such an overview is essential to have proper perspec- America, and Karl Niklas, the long-term Editor-in-Chief of the tive on the origin and phylogenetic relationships of land plants American Journal of Botany, jointly asked the three of us to and the many diverse groups of ``algae,'' as well as those serve as guest editors for a special issue devoted to the re- otherwise unrelated groups (especially fungi) that nonetheless markable recent progress in reconstructing the evolutionary have traditionally been allied with plants and which are still history of plant life, also known as the plant tree of life. Our part of the purview of this journal and its governing society. invitations to prospective authors went out in June of 2003. The group-speci®c authors were given free rein as to how to For this issue to appear in print only 16 months later, with approach and cover their groups. Thus, you will see a wide 100% delivery of solicited articles and each of them outstand- range of treatments. The central, common thread, however, to ing, is nothing short of remarkable. This testi®es to the com- all 11 of these articles is a description, usually encompassing mitment and enthusiasm of the authors; to the editorial exper- a critical assessment, of our current state of understanding of tise and dedication of Karl Niklas, the journal's of®ce manager the phylogeny of each group. Although this phylogenetic un- Caroline Spellman, copy editor Beth Hazen, and production derstanding increasingly relies on gene sequence data, many editors Beth Hazen and Elizabeth Lawson; and to the timely of the articles also provide a more or less thorough integration cooperation of the two to four expert scientists chosen to pro- of phylogeny with the overall evolution (principally from a vide rigorous, anonymous, and speedy review of each article. morphological standpoint) and classi®cation of the group in Although the rapid gestation of this issue ensures that it is up- question. to-date and timely, these articles should also, we believe, prove The coverage represented by the 11 taxon-speci®c papers to be of relatively long-lasting and enduring value. We trust re¯ects the amount of effort and progress made in elucidating that readers of this ®rst-ever special issue of this journal will the phylogeny of each group, as well as their size and eco- be as delighted with the outcome of this effort as are we. nomic and ecological importance. Thus, angiosperms, the larg- est, most important, and best studied group of land plants, are NATURE OF THE ARTICLES IN THIS ISSUE covered by three articles (Soltis and Soltis, 2004; Chase, 2004; Judd and Olmstead, 2004), whereas three much smaller but The other 18 articles in this issue fall into two general cat- considerably older groups of land plantsÐseed plants (Bur- egories. Twelve are taxon-oriented, while the other six are top- leigh and Mathews, 2004), ferns (Pryer et al., 2004), and bryo- ical in nature. Of the ®rst set, 11 are taxon-speci®c, providing phytes (Shaw and Renzaglia, 2004)Ðare each given but a sin- broad coverage of current understanding of the phylogeny and gle article. Likewise, green algae, the parent group of land overall evolution of the major groups of ``plants,'' as de®ned plants, are treated in a single paper (Lewis and McCourt, either phylogenetically or historically. The twelfth, by Keeling 2004), as are the sister group to green algae/land plants, the (2004), was commissioned to provide a broad overview of red algae (Saunders and Hommersand 2004). Two papers cov- er three of the largest and best studied groups of secondary 1 Manuscript received 29 June 2004; revision accepted 2 July 2004. plastid-containing algae, the dino¯agellates (Hackett et al., We wish to thank all those responsible for helping put together this special 2004) and the putatively related heterokonts (brown algae, di- issue of this journal, including the journal's editor-in-chief Karl Niklas, its of®ce manager Caroline Spellman, its copy editor Beth Hazen, its production atoms, chrysophytes, etc.) and haptophytes (Andersen, 2004). editor Elizabeth Lawson, and, of course, the many authors of the various Finally, Lutzoni et al. (2004) take on all the fungi. Page limits papers that comprise the issue. We also thank Gordon Burleigh, Chuck Del- to this issue made for hard choices, and we regret that four wiche, Les Goertzen, Patrick Keeling, Sarah Mathews, Kathleen Pryer, and fascinating but mostly poorly studied groups with secondary SasÏa Stefanovic for comments on this manuscript, Walt Judd and Patrick Keel- plastids (apicomplexans, chlorarachniophytes, cryptomonads, ing for communicating unpublished data, and the US National Institutes of and euglenids), as well the primary plastid-containing glau- Health (JDP), US National Science Foundation (DES and MWC), and the Royal Botanic Gardens, Kew (MWC), for funding to study plant phylogeny cophytes, could be given only brief mention in the overview and genome evolution. by Keeling (2004). 5 E-mail: [email protected]. With three exceptions, all 12 taxon-oriented articles are es- 1437 1438 AMERICAN JOURNAL OF BOTANY [Vol. 91 sentially review articles, providing a critical overview and syn- taining plastids). As described in the next paragraph, this is thesis of the recent literature pertinent to their respective sub- necessarily set in the broader context of overall eukaryotic jects. The article by Lutzoni et al. (2004) on fungal phylogeny phylogeny. Figure 2 shows our estimate of both phylogenetic is the ®rst paper from a large team of investigators whose relationships and divergence times of extant land plants. These currently funded goal (from the U.S. National Science Foun- trees are based entirely on DNA sequence data, generated and dation Tree-of-Life Program) is to reconstruct phylogenetic re- analyzed in far too many studies to cite in this brief overview lationships of 1500 fungi using eight genes (ca. 10 kb of DNA (for speci®c citations, see the 12 taxon-oriented articles in this sequence) and represents a major achievement in fungal phy- issue and references therein). We emphasize that these trees logeny akin to the earlier large-scale collaborative molecular are an estimate of phylogenyÐof evolutionary historyÐand, studies on angiosperms (e.g., Chase et al., 1993; Soltis et al., in the case of the global tree (Fig. 1), of only one dimension 2000). The article by Pryer et al. (2004) on fern phylogeny at that, of branching order (but not divergence time). As with stands out among all of the papers in this issue by virtue of all science, we can never be certain we have obtained ``the presenting the only fully integrated study of both the branch- truth.'' At the same time, however, the power of the DNA ing pattern and divergence times of a particular group of revolution makes it likely that we will soon approach relatively plants, both derived from the same set of gene sequence data. great certainty in estimating most or all of the branching orders The article by Burleigh and Mathews (2004) on seed plant of extant plant phylogeny and will gradually achieve greater phylogeny establishes a seemingly robust framework tree for and greater understanding of the time dimension as well. Im- gymnosperms and provides important evidence for the single portantly, as Crane et al. (2004) and Crepet et al. (2004) cau- most controversial and revolutionary hypothesis generated tion, a more complete understanding of the tree of life can from molecular analyses of any group of plants, namely, that only be accomplished with the integration of fossils. conifers are paraphyletic, with Gnetales sister to Pinaceae to As reviewed by Keeling (2004), at its deepest level, the the exclusion of all other conifers. Although these three arti- history of plants is a history of endosymbiosis, of their birth cles largely focus on new molecular data sets and phylogenetic by primary, eukaryotic/cyanobacterial endosymbiosis and of analyses, in keeping with the nature of this issue, the authors multiple secondary, tertiary, etc., eukaryotic/eukaryotic endo- have also broadened their remit beyond that of the usual orig- symbioses that have spread plastids into several other regions inal article, to provide a somewhat longer than normal over- of the eukaryotic world. Endosymbiosis dominates our global view of the group in question. perspective of plant evolution, as portrayed in Fig. 1. Of the The six topical articles focus on selected issues that are ®ve supergroups of eukaryotes tentatively identi®ed by Keel- highly relevant to reconstructing and understanding the plant ing (2004) and mapped onto Fig.
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