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    • The Plant Tree of Life: An Overview and Some Points of ViewAuthor(s): Jeffrey D. Palmer, Douglas E. Soltis, Mark W. ChaseReviewed work(s):Source: American Journal of Botany, Vol. 91, No. 10 (Oct., 2004), pp. 1437-1445Published by: Botanical Society of AmericaStable URL: http://www.jstor.org/stable/4123845 .Accessed: 17/02/2012 02:04Your use of the JSTOR archive indicates your acceptance of the Terms & Conditions of Use, available at .http://www.jstor.org/page/info/about/policies/terms.jspJSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range ofcontent in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new formsof scholarship. For more information about JSTOR, please contact support@jstor.org. Botanical Society of America is collaborating with JSTOR to digitize, preserve and extend access to American Journal of Botany.http://www.jstor.org
    • American Journalof Botany 91(10): 1437-1445. 2004. THE PLANT TREE OF LIFE: AN OVERVIEW AND SOME POINTS OF VIEW JEFFREYD. PALMER,2,5DOUGLAS E. SOLTIS,3 AND MARK W. CHASE4 of 2Department Biology, IndianaUniversity, Bloomington, Indiana47405-3700 USA; 3Department Botany and the Genetics of Institute, University of Florida, Gainesville, Florida 32611 USA; and 4MolecularSystematics 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 natureof its articles. We then presentour 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 accuratelydated plant tree of life and the importanceof such a grandendeavor. Key words: algae; endosymbiosis; Gnepines hypothesis; land plants; phylogeny; plastids. To mark the 90th anniversaryof this journal, Scott Russell, eukaryoticphylogeny and plastid primaryand secondarysym-the then-ImmediatePast Presidentof the Botanical Society of biosis. Such an overview is essential to have proper perspec-America, and KarlNiklas, the long-termEditor-in-Chief the of tive on the origin and phylogenetic relationshipsof land plantsAmerican Journal of Botany, jointly asked the three of us to and the many diverse groups of "algae," as well as thoseserve as guest editors for a special issue devoted to the re- otherwise unrelatedgroups (especially fungi) that nonethelessmarkable recent progress in reconstructingthe evolutionary have traditionallybeen allied with plants and which are stillhistory 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-specific authorswere given free rein as to how toFor this issue to appear in print only 16 months later, with approachand cover their groups. Thus, you will see a wide100% delivery of solicited articles and each of them outstand- range of treatments.The central, common thread,however,toing, is nothing short of remarkable.This testifies to the com- all 11 of these articles is a description,usually encompassingmitment and enthusiasmof the authors;to the editorialexper- a critical assessment, of our currentstate of understanding oftise and dedicationof KarlNiklas, the journalsoffice manager the phylogeny of each group. Although this phylogenetic un-Caroline Spellman, copy editor Beth Hazen, and production derstandingincreasingly relies on gene sequence data, manyeditors Beth Hazen and Elizabeth Lawson; and to the timely of the articles also provide a more or less thoroughintegrationcooperationof the two to four expert scientists chosen to pro- of phylogeny with the overall evolution (principally from avide rigorous, anonymous, and speedy review of each article. morphological standpoint) and classification of the group inAlthough 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 representedby the 11 taxon-specific papersto be of relatively long-lasting and enduring value. We trust reflects the amount of effort and progress made in elucidatingthat readers of this first-everspecial 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 ARTICLESIN 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 plants-seed plants (Bur-egories. Twelve are taxon-oriented,while the other six are top- leigh and Mathews, 2004), ferns (Pryeret al., 2004), and bryo-ical in nature.Of the first set, 11 are taxon-specific,providing phytes (Shaw and Renzaglia, 2004)-are each given but a sin- ofbroad coverage of currentunderstanding the phylogeny and gle article. Likewise, green algae, the parent group of landoverall evolution of the major groups of "plants," as defined 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 (Saundersand Hommersand2004). Two paperscov- er three of the largest and best studied groups of secondary Manuscriptreceived 29 June 2004; revision accepted 2 July 2004. plastid-containing algae, the dinoflagellates (Hackett et al., We wish to thank all those responsible for helping put together this specialissue of this journal, including the journals editor-in-chief Karl Niklas, its 2004) and the putatively related heterokonts(brown algae, di-office managerCaroline 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 limitspapers that comprise the issue. We also thank Gordon Burleigh, Chuck Del- to this issue made for hard choices, and we regret that fourwiche, Les Goertzen, Patrick Keeling, Sarah Mathews, Kathleen Pryer, and fascinating but mostly poorly studied groups with secondarySaia Stefanovidfor comments on this manuscript, WaltJuddand PatrickKeel- plastids (apicomplexans, chlorarachniophytes, cryptomonads,ing for communicating unpublisheddata, and the US National Institutes of and euglenids), as well the primary plastid-containingglau-Health (JDP), US National Science Foundation (DES and MWC), and theRoyal Botanic Gardens,Kew (MWC), for funding to study plant phylogeny cophytes, could be given only brief mention in the overviewand genome evolution. by Keeling (2004). SE-mail:jpalmer@bio.indiana.edu. With three exceptions, all 12 taxon-orientedarticles are es- 1437
    • 1438 AMERICAN JOURNALOF BOTANY [Vol. 91sentially review articles,providinga criticaloverview and syn- taining plastids). As described in the next paragraph,this isthesis of the recent literaturepertinentto their respective sub- necessarily set in the broader context of overall eukaryoticjects. The article by Lutzoni et al. (2004) on fungal phylogeny phylogeny. Figure 2 shows our estimate of both phylogeneticis the first paper from a large team of investigators whose relationshipsand divergence times of extant land plants.Thesecurrentlyfunded goal (from the U.S. National Science Foun- trees are based entirely on DNA sequence data, generatedanddationTree-of-LifeProgram)is to reconstructphylogeneticre- analyzed in far too many studies to cite in this brief overviewlationshipsof 1500 fungi using eight genes (ca. 10 kb of DNA (for specific citations, see the 12 taxon-orientedarticlesin thissequence) and representsa major achievement in fungal phy- issue and references therein). We emphasize that these treeslogeny akin to the earlier large-scale collaborativemolecular are an estimate of phylogeny-of evolutionary history-and,studies on angiosperms (e.g., Chase et al., 1993; Soltis et al., in the case of the global tree (Fig. 1), of only one dimension2000). The article by Pryer et al. (2004) on fern phylogeny at that, of branchingorder (but not divergence time). As withstands out among all of the papers in this issue by virtue of all science, we can never be certain we have obtained "thepresentingthe only fully integratedstudy of both the branch- truth." At the same time, however, the power of the DNAing pattern and divergence times of a particular group of revolutionmakes it likely thatwe will soon approachrelativelyplants, both derived from the same set of gene sequence data. great certaintyin estimatingmost or all of the branchingordersThe article by Burleigh and Mathews (2004) on seed plant of extant plant phylogeny and will gradually achieve greaterphylogeny establishes a seemingly robust frameworktree for and greaterunderstanding the time dimension as well. Im- ofgymnospermsand provides importantevidence for the single portantly,as Craneet al. (2004) and Crepet et al. (2004) cau-most controversial and revolutionary hypothesis generated tion, a more complete understandingof the tree of life canfrom molecular analyses of any group of plants, namely, that only be accomplished with the integrationof fossils.conifers are paraphyletic,with Gnetales sister to Pinaceae to As reviewed by Keeling (2004), at its deepest level, thethe exclusion of all other conifers. Although these three arti- history of plants is a history of endosymbiosis, of their birthcles largely focus on new moleculardata sets and phylogenetic by primary, eukaryotic/cyanobacterial endosymbiosis and ofanalyses, in keeping with the natureof this issue, the authors multiple secondary, tertiary,etc., eukaryotic/eukaryotic endo-have also broadenedtheir remit beyond that of the usual orig- symbioses that have spreadplastids into several other regionsinal article, to provide a somewhat longer than normal over- of the eukaryoticworld. Endosymbiosis dominates our globalview of the group in question. perspective of plant evolution, as portrayedin Fig. 1. Of the The six topical articles focus on selected issues that are five supergroupsof eukaryotes tentatively identified by Keel-highly relevant to reconstructingand understanding plantthe ing (2004) and mapped onto Fig. 1, two, Primoplantaeandtree of life. Crane et al. (2004) emphasize the importanceof Chromoalveolates,are largely if not entirely defined by a his-integratingfossil evidence with data, both morphologicaland tory of endosymbiosis. The Primoplantaewere by definitionmolecular, from extant plants, and also stress that a compre- born of primary, cyanobacterial endosymbiosis, and thehensive understandingof some groups (e.g., seed plants) will Chromalveolateswere possibly born of red algal secondaryrequire a thorough reassessment of available fossils. Kellogg symbiosis (and if not, were then repeatedly subjected to redand Bennetzen (2004) review the structure,evolution, and, toa limited extent, phylogenetic utility of plant nucleargenomes. algal symbiosis; discussed later and Fig. 1). Two of the other three supergroupsof eukaryotes have also acquired plastidsLinderand Rieseberg (2004) discuss the increasinglypowerful and evolved "plantlike" attributesthrough secondary symbi- molecular approachesused to dissect the role of hybridization in plant evolution. Whereas almost all articles in this issue osis, both times via green algae endosymbionts (Fig. 1). focus on reconstructingthe branchingpattern(or, sometimes, Although whole-organism symbiosis represents horizontal the network) of plant evolutionary history, Sanderson et al. gene transfer (HGT) on the grandest scale possible, there is little reason to suspect that HGT occurs commonly enough (2004) and Crepet et al. (2004) explore a relatively recent de- within eukaryotic evolution to compromise significantly our velopment in molecular phylogenetics, albeit one that we ex- pect to achieve great importance, namely, the application of prospects for recovering the metaphoricalplant tree of life. In the prokaryoticworld, in contrast, HGT has shaken the very gene sequence data to estimate divergence times. Crepetet al. (2004) do so as part of a broader,original effort to integrate concept of whether an underlying tree structureexists to re- the fossil record more thoroughly with the molecular record. cover, the metaphorof a networkof gene trees being preferred Sanderson et al. (2004) note that despite the limitations of by some authorities(Gogarten et al., 2002). As noted in the methods for estimating divergence times, recent analyses are next section, the prevalenceof HGT in the bacterial,including converging on similar and reasonable age estimates of angio- cyanobacterial, world may provide important limits on our sperms. Finally, Friedman et al. (2004) provide a timely re- ability to answer some of the deepest, most fundamentalques- view of a topic of rapidly growing interest in plant biology, tions about the origin and earliest evolution of plants/plastids. namely, the evolution of plant development. The view of land plant phylogeny expressed in Fig. 2 has Although these articles do not cover every possible topic several messages. It tells us that most of the major groups of and group that are relevant to efforts to reconstructand inter- extant land plants are monophyletic. Extant angiosperms are pret the plant tree of life, we believe that in sum they provide monophyletic, as are gymnosperms, seed plants, ferns (albeit sufficiently broad and deep coverage to give a vivid sense of slightly broadenedto include horsetails), euphyllophytes, ly- the excitement, progress, questions, and prospects in this im- cophytes, and vascularplants. Bryophytes, shown unresolved, portantand booming area of botanical research. are the conspicuous exception here, most likely being a grade that is paraphyleticto vascular plants (Shaw and Renzaglia, THE PLANT TREE OF LIFE: A 2004 ESTIMATE 2004). Figure 2 emphasizes how asymmetricthe tree of extant Figure 1 shows our currentestimate of the overall relation- plant life is with respect to species richness. At the extreme,ships of extant "plants" (defined here as all organisms con- Amborella trichopoda, a single species endemic to New Ca-
    • October 2004] PALMER AL.-OVERVIEWOF PLANTTOL ET 1439 Lewis&McCourt Originof U plastids by cyanobacterial - 0 - endosymbiosis 0 m Sers& Hommersand rn. of Origin 0 =o mitochondria by a-proteobacterial endosymbiosis o CD CD C) -ittal. et - Fig. 1. Cladogram showing phylogenetic relationshipsamong the major groups of extant eukaryotes, with emphasis on plastid-containinggroups and theirevolutionary connections via primary and secondary endosymbiosis. This estimate of relationshipsis modified from Keeling (2004) and Baldauf et al. (2004),which should be consulted for more inclusive trees showing additional groups of nonphotosyntheticeukaryotes. The names and circumscriptionsof the fiveeukaryotic supergroups(Excavates, etc.) are from Keeling (2004), except that we have used "Primoplantae"(J. D. Palmer,unpublished manuscript)in placeof "Plants." Colors distinguish the three lineages of primary plastid-containingeukaryotes (Primoplantae)and also mark those eukaryotes with secondaryplastids of red or green algal origin. The exact placement of the "symbiosis" arrows is arbitrary;essentially nothing is currently known about the timing ofthese events or the specific nature of the donor lineages. Two, probably independent,green algal secondary symbioses are shown, whereas the number of redalgal symbioses could be as few as one (as shown) or, less likely, as many as five (see text). The three slashes indicate loss of plastids under the hypothesis ofa single early red algal secondary symbiosis and Chromalveolate monophyly. "Other charophytes" denotes what is most likely a grade of four orders fromwhich the Charales/landplant clade has arisen (Karol et al., 2001; Lewis and McCourt, 2004). Groups covered by a particulararticle in this special issue arecircled and connected to the names of the articles authors. Branch lengths in this cladogram are entirely arbitrary;no implications with respect to time areintended.ledonia, is probably the sister group to all other living angio- at the base of several major groups-angiosperms, gymno-sperms, numberingover 250 000 species. Similar asymmetries sperms, and ferns-implies relatively rapid emergence of theare evident at various places on the tree (Fig. 2), making it major lineages of each group from a common ancestor.Mostclear that rates of speciation and extinction vary widely over of the diversity of these clades is not, however, representedontime and from group to group. The series of short internodes this tree. For species-rich groups such as the eudicots and
    • 1440 AMERICAN JOURNAL OF BOTANY [Vol. 91 Chase Judd&Olmstead Soltis&Soltis Burleigh Mathews & Eudicots 175,000 Monocots 70,000 Chloranthaceae 70 Ceratophyllaceae 6 ? Magnoliids 9,000 Austrobaileyales 100 0 Nymphaeaceae 70 v Amborellaceae 1 roo m C < 220 SPinaceae Gnetales 80 Other conifers 400 SGinkgo 1 Cycads 130 11,000 Horsetails 15 on Marattioidferns 240 "1 Ophioglossoidferns 110 Whiskferns 15 Lycophytes 1,200 Pryer et a Mosses 15,000 0 Liverworts 9,000 = Shaw &Renzaglia Hornworts 100 ORD SIL DEV CARB IPERM TRI I JURASSICICRETACEOUSI TERTIARY I PALEOZOIC MESOZOIC CENOZOIC 500 400 300 200 100 0 Fig. 2. Chronogramshowing estimates of phylogenetic relationships and divergence times among the major groups of extant land plants. The estimate ofrelationships is synthesized from the following papers in this issue: Burleigh and Mathews (2004), Pryer et al. (2004), Shaw and Renzaglia (2004), and Soltisand Soltis (2004). Divergence time estimates are mostly based on analyses of molecular data with fossil constraints(Wikstr6met al., 2001; Pryer et al., 2004)and are augmented by fossil evidence (Kenrick and Crane, 1997; Wellman et al., 2003). Estimates of the number of species in each group are from Judd et al.(2002) and W. S. Judd (personal communication). Groups covered by a particulararticle in this special issue are circled and connected to the names of thearticles authors. "Other conifers" refers to the clade consisting of all conifers except for Pinaceae (see Burleigh and Mathews, 2004). "Lepto. ferns" refers toleptosporangiateferns.monocots, we can barely imagine how many more finely 2004) speaks volumes to the power of thousands of (nucleo-spaced internodes must exist to account for the vast number tide) characters,and of judicious taxon sampling, to resolveof extant species in these groups. That so much progress has close divergences and heralds success in ultimately resolvingalreadybeen made in resolving many of these internodes(e.g., all but the most rapid and anciently compressed of radiationssee Chase, 2004, on resolving the backbone of the monocot as data sets head towards the tens and even hundredsof thou-tree; also see Judd and Olmstead, 2004, and Soltis and Soltis, sands of characters.
    • October 2004] PALMER AL.-OVERVIEWOF PLANT ET TOL 1441 TOPOLOGICALCONTROVERSIES THE PLANT IN bacteria (Zhaxbayevaet al., 2004) to bedevil attemptsto ever TREE OF LIFE completely settle the issue of how many primary plastid ori- gins and, especially, to identify the cyanobacterialprogeni- Although the papers in this issue amply document and re- tor(s) of plastids.view the great progressmade in recent years in elucidatingtheplant tree of life, thereis of course much work still to be done. What happened after plastids arose?-If plastids did in-Many plant groups have barely been touched by phylogenetic deed arise only once, then a major ensuing issue is, what isinquiry, and for otherslittle resolutionhas been obtained.Even the branchingorderamong the three lineages of Primoplantae?in such a well-studied group as angiosperms,much important Keeling (2004) summarizes evidence that leads him to con-work remains, and not just at the tips of the trees where most clude that it "seems likely" that the glaucophytesare sister tospecies-level problems await resolution in this immense clade green algae plus red algae (as shown in Fig. 1), whereas weof over 250 000 species. For example, Soltis and Soltis (2004) view the issue as largely unsettled. The strongest support forpoint out a number of major groups within angiosperms for this relationship among plastid genes has always come fromwhich significantresolutionis currentlylacking. These include plastid small subunit rDNA (e.g., Turneret al., 1999). How-not only the deep level pentachotomy shown in Fig. 2 (of ever, a recent analysis of plastid large subunit rDNA, eithereudicots, monocots, Chloranthaceae, Ceratophyllaceae, and alone or, more importantly,in combinationwith small subunitmagnoliids), but also the major groups that make up the im- rDNA, finds instead strong (99% bootstrap)supportfor greenmense (175 000 species) clade known as eudicots. algae as sister to red algae plus glaucophytes (S. Turner,K. We will not discuss any furtherthese many areas of non- M. Pryer,and J. D. Palmer,unpublisheddata). Although mostcontroversial poor resolution. Likewise, we will not explore analyses of very large charactersets (of ca. 40 plastid proteinhere any of the major methodological controversies that sur- genes) find strong support for glaucophytes being "deepest"round the business of inferringthe plant tree of life. Some of (e.g., Martinet al., 2002), at least one is essentially unresolvedthese are, however, touched on in the following sections on on this issue (Turmelet al., 1999). Critically,all such analysescase studies of topological controversy,and include such top- are plagued by woefully inadequatetaxon sampling (only aics as the appropriategeneration and use of DNA vs. other single glaucophyte, a single cyanobacterialoutgroup,and justevidence in inferring phylogeny (e.g., Scotland et al., 2003), a few each of red and green algae), which, especially at thistrade-offs between sampling more taxa vs. more characters level of divergence, raises the specter of obtainingstrong sup-(Chase et al., 1993; Soltis et al., 2004), the limits and pitfalls port for an incorrect topology (Soltis et al., 2004). Althoughof using moleculardata to date plant divergence times (Crepet the only relevant nuclear multigene analysis appears to lacket al., 2004; Sandersonet al., 2004), and how best to construct resolution on this issue (Moreira et al., 2000), red and greenand assess phylogenetic trees from DNA sequence data (Fel- algae do share a nuclear gene duplication/plastidtargetingsenstein, 2004; Albert, 2005). Instead we focus on six current event to the exclusion of glaucophytes (Rogers and Keeling,controversiesin plant phylogeny, chosen because they all con- 2003).cern deep and importantissues in plant evolutionary history, Many more sequence data (especially from glaucophytes)relate to taxa shown in Figs. 1 and 2, and illustrate a variety are clearly needed to resolve this key issue, which greatly af-of biological and methodological issues in phylogeny recon- fects interpretation various importantaspects of plastidevo- ofstruction. lution, such as their history of gene loss (Martinet al., 2002) and cell wall loss. For example, glaucophytes uniquely retain How many origins of plastids/plants?-The two deepest a bacterial-like,peptidoglycan cell wall aroundtheir plastids:questions in plant phylogeny concern the birth of plastids/ Did green and red plastids lose their cell wall independentlyplants via cyanobacterial endosymbiosis: Did plastids arise or in a common ancestor? Unfortunately,the apparentpredi-once or more than once, i.e., was there but a single or as many lection of cyanobacteria(the only good outgroupsfor this in-as three cyanobacterialendosymbioses to establish the three quiry) to engage in HGT (Zhaxbayevaet al., 2004) compro-lineages of clearly monophyletic, primary plastid-containing mises, perhapsseverely or even irrevocably,our ability to an-eukaryotes (green algae, red algae, and glaucophytes)? And swer this question.relatedly, which lineage(s) of cyanobacteriagave rise to plas-tids? Although we have no clue of an answer to the second How many secondary symbioses of red algae?-Perhapsquestion, longstanding controversy over the former has sub- the most importantquestion relating to the symbiotic historysided over the past decade. This is because DNA sequence- of plastids concerns the number of red algal secondary sym-based trees and a number of features of plastid genomes, the bioses. The diversity of eukaryoteswith secondaryred plastidsplastid protein import apparatus,and photosyntheticpigment is immense, and these are phylogenetically interspersedwithproteins have converged to provide clear (to some observers, groups that lack plastids (Fig. 1). This has led many observersoverwhelming) evidence for a single origin of plastids (Fig. to postulate multiple secondary symbioses involving a red al-1; Palmer, 2003; Keeling, 2004; McFadden and van Dooren, gal endosymbiont. As reviewed by Keeling (2004), however,2004), although there are still reasons (Palmer,2003; Stiller, recent DNA evidence, both sequence-based and rearrange-2003; Stiller et al., 2003) to be cautious in assuming that this ment-based, now provides reason to think that all secondaryissue is completely settled. It should also be emphasized that red algal plastids trace back to a common secondarysymbiosisthe evidence for a common origin of plastids is much stronger (Fig. 1, red arrow), in the common ancestor of a putative eu-for green and red algae than for the comparativelypoorly stud- karyotic supergroup-Chromalveolates-first postulated byied glaucophytes (only a single glaucophyte plastid genome Cavalier-Smith(1998). If Chromalveolatesare indeed mono-has been sequencedand scant informationis availableon glau- phyletic, arising by only a single red algae symbosis, then thiscophyte nuclear and mitochondrialgenomes). Although very means that the many diverse lineages within the group thatrare in plastids, HGT may be sufficiently common in cyano- apparently lack plastids (see Keeling, 2004, for many such
    • 1442 AMERICAN JOURNALOF BOTANY [Vol. 91examples beyond the three shown in Fig. 1) must have once Figure 2 shows a number of surprisingplacements and re-had them. In the case of ciliates and oomycetes (Fig. 1), initial lationshipsthat have emerged solely from and/orfound stronganalysis of complete nuclear genomes has failed to find any supportonly from DNA sequences. Withinferns, these includesignificant vestiges of putative plastid-derived genes (P. J. the placement of horsetails within the ferns and the sister-Keeling, University of British Columbia, personal communi- group relationshipof the enigmatic, vegetatively reducedPsi-cation). Either ciliates and oomycetes have been cleansed of lotales and the ophioglossoid ferns (Pryeret al., 2004). Withintheir plastid heritage to an extent unthinkablefor land plants angiosperms, we note the deep positions of the monotypic,(Martinet al., 2002) or else the evidence for Chromalveolate New Calendonian-endemic, Amborellaceae,and of Nymphae-monophyly and a single red algal secondary symbiosis is mis- aceae and Austrobaileyales(Soltis and Soltis, 2004). Also notleading. Clearly, much more phylogenetic and genomic evi- shown are the many other surprising placements that havedence is needed. emerged within groupsof land plants (and also nonlandplants) not covered by the obviously scanty representationafforded Where does Mesostigma belong?-As reviewed by Lewis by these two global, frameworktrees. In almost all these cases,and McCourt(2004), a majorpuzzle in green algal phylogeny however, the surprisehas been one of delight ("Ah ha, weveconcerns the placement of Mesostigma, an unusual asymmet- finally found a place for that troublesome species X.") ratherrical unicell. With good taxon sampling, a four-gene, three- than one of dismay or disbelief ("Theres no way species Ygenome data set strongly supportsMesostigma within charo- belongs in that group; something has got to be wrong withphytes, probablyas sister to the rest of this clade (Karolet al., these DNA data."). Frequently, careful assessment of mor-2001), whereas a two-gene plastid data set places it with equal- phology reveals characters that agree with the "DNA sur-ly strong support as sister to all green algae, prior to what is prise," although in many instances these charactersmay beotherwise regardedas the fundamentalsplit in green algal evo- cryptic (Judd and Olmstead, 2004).lution (between charophytesand chlorophytes;Turmelet al.,2002a; Fig. 1). With poor taxon sampling, a similar conflict Are Gnetales really sister to Pinaceae?-The most radical,arises for much larger charactersets. Some analyses of com- shocking, and controversialplacement of any group of plantsbined matricesof ca. 40 plastid genes place Mesostigmawithin concerns Gnetales, a small, relatively obscure group of gym-the charophytes(e.g., Martinet al., 2002), whereas other such nosperms. Whereas a notable hypothesis from morphologicalanalyses and those of 19 mitochondrialgenes place it as sister cladistic studies had been that Gnetales were sister to angio-to all other green algae (Lemieux et al., 2000; Turmelet al., sperms, many molecular studies instead found gymnosperms2002b). As with many critical phylogenetic issues in plants to be monophyletic and placed Gnetales within conifers, asand other organisms, robust resolution of the position of Me- sister to Pinaceae (e.g., Bowe et al., 2000; Chaw et al., 2000;sostigma may requireboth large charactersets and bettertaxon reviewed in Burleigh and Mathews, 2004). Although othersampling. Resolving the placementof Mesostigmais important molecular studies found support for monophyly of conifersto understanding early evolution of green algae, as well as the and instead placed Gnetales either as sister to conifers or asevolutionary trendsin organellargene content (Lemieux et al., sister to all other seed plants, the original analyses in the paper2000; Turmel et al., 2002b) and photosynthetic pigments by Burleigh and Mathews (2004) in this issue provide strong(Yoshii et al., 2003). evidence for the "gnepines" hypothesis (Bowe et al., 2000; Chaw et al., 2000), i.e., that Gnetales and Pinaceae are sister Whos at the base of land plants?-A major controversy taxa. Burleigh and Mathews (2004) sampled moderately ex-in land plant phylogeny concerns the base of the tree (Fig. 2). tensively within gymnospermsand examined more genes (13Traditionally,land plants have been divided into two groups, total; five plastid, four nuclear, and four mitochondrial)andvascular plants and bryophytes. Although vascular plants are characters(almost 19000 nucleotides) than in any other pre-strongly supportedas monophyletic based on both DNA evi- vious study on this issue. Contraryto previous claims (e.g.,dence (e.g., Nickrent et al., 2000) and morphology (Kenrick Rydin et al., 2002) that earlier,three-genomeanalyses favoringand Crane, 1997), bryophytes are now generally thought to the gnepines topology rested "almost exclusively" on mito-comprise a grade of three monophyletic lineages (mosses, liv- chondrial genes and that there is a "severe conflict betweenerworts, and hornworts)of uncertainrelationshipto each other the mitochondrialand other genomes [that]should not be sup-and to vascular plants. Many studies (listed in Shaw and Ren- pressed or ignored," Burleigh and Mathews (2004) found thatzaglia, 2004) have addressed these relationships.In our view all three genomic data partitionssupportthe gnepines result.there is as yet no clear answer,and thereforewe show the base This was true in all maximumlikelihood analyses and in thoseof land plants as a tetrachotomy (Fig. 2). Most commonly, parsimony analyses in which the most rapidly evolving siteseither liverworts or hornworts emerge as sister to all land were excluded. Indeed, contra Rydin et al. (2002), the mito-plants, but we see little reason to favor one result over the chondrialpartitionactually provided only slightly lower boot-other based on currentdata. Those who do, e.g., favoring liv- strap supportfor gnepines in these analyses than did the nu-erworts-sisteron the basis of "compelling evidence" (Fried- clear or plastid partitions.Moreover,when all 13 genes wereman et al., 2004) from so-called "raregenomic markers"(mi- combined (and with the fastest sites excluded for parsimony),tochondrial intron presence/absence; Qiu et al., 1998; Dom- both parsimonyand maximumlikelihood gave 100%bootstrapbrovska and Qiu, 2004) are in our view privileging a select supportfor gnepines.few (not so rarelychanging) charactersover thousandsof other Only in parsimonyanalyses that included all sites did Bur-characters for which we have a long history of robust use. leigh and Mathews (2004) fail to recover the gnepines topol-Such purportedlyrare events can be subject to high levels of ogy. Tellingly, however, these analyses (with all 13 genes)homoplasy when examined with intensive sampling (Adams placed Gnetales in a radically different position, as sister toet al., 2002; McPhersonet al., 2004), and thus we do not really all other seed plants, promptingBurleigh and.Mathews(2004)know how reliable any of these sorts of charactersare. to conclude that the "Gnetales-sistersignal is restrictedto sites
    • October 2004] PALMER AL.-OVERVIEW PLANT ET OF TOL 1443[largely in plastid genes] in the fastest two of nine evolution- (Chase, 2004; Judd and Olmstead, 2004; Soltis and Soltis,ary rate categories" and reflects bias "in the most rapidly 2004).evolving sites to which parsimony is particularlysensitive." The next 20 years will undoubtedlysee an ever more rapidIn short, the Gnetales-sisterplacement is a likely example of accumulation of DNA sequence data and the generation oflong-branch-attraction (between the long branches leading to comprehensive,robustly resolved, and increasinglywell-datedGnetales and to the outgroups), and the gnepines topology is phylogenetic trees. Phylogenetics is now hitched to a powerfullikely to be correct.Nonetheless, we also cautionthatthis issue engine-the economic, largely biomedical engine that hasshould not be considered settled; even though receiving 100% been driving the development of faster and cheaper technol-bootstrap support in most 13-gene analyses, the gnepines to- ogies for sequencing DNA and for high-throughputroboticpology is, as Burleigh and Mathews (2004) point out, "very handling of DNA in general. Even at the currentrate of datasimilar" to the gnetifer topology (Gnetales sister to a mono- accumulation,nearly all of the remaining problems in plantsphyletic conifers) "and potentially even a small amount of are tractable, and it is likely that there will continue to beerroror bias could influence [these] phylogenetic results." improvements that will increase output and hasten progress. We emphasize this particularcase because it nicely illus- The next 20 years may even see radical breakthroughs se- intrates a variety of issues in phylogenetics. It illustrates the quencing and other DNA technologies, breakthroughsthatpotential to get artifactual results (e.g., the Gnetales-sister could allow the virtually limitless collection of gene and evenplacement) under the following evolutionary conditions: (1) whole genome data from most plants (especially from thehigh levels of extinction (on, among others, the outgroup small but gene-rich genome of plastids). If so, then we willbranchand the branchesleading to Gnetales, angiosperms,and certainly look back on this era as a small waystation on theGinkgo), (2) high rates of sequence evolution (in Gnetales), path toward reconstructingthe complex and fascinating evo-and (3) biased evolution at a subset of sites (rapidlyevolving lutionary history of the botanical world.sites in plastid and nuclear genes). The first two of these fac- The prospects for achieving a robustly resolved and well-tors-extensive extinction and rapid sequence evolution-are dated tree of plant life are exhilarating.To rephraseDobzhan-probably the greatest intrinsic problems in molecular phylo- sky (1973), "Nothing in biology makes sense except in lightgenetics, especially when operating in concert, as with the of phylogeny." Only with an accurate tree in hand can weGnetales placement.This case vividly illustrateshow different properlymake sense of the profoundrichness and diversity ofpartitionsof a sequence data set can generatehighly supported the botanical world. Only then can we fully appreciateevo-trees with radically different topologies and also points to an lution at all levels of organization, from the ecological andapparentlyuseful methodological approach to deal with this morphological to the biochemical and genomic. Specific ap-intragenicconflict. It also illustratesthe superiorperformance plications of phylogenetic studies, of "tree thinking," are tooof maximum likelihood over parsimonyunder these challeng- numerous to list here, ranging from the applied (Yates et al.,ing conditions (whereas parsimonygenerally performswell in 2004) to fundamentalstudies of evolutionary and ecologicalsituationswhere extinction has not eliminatedthe potentialfor processes (36 such applications are listed in Table 3.1 of Fu-extensive taxon sampling to break up the long branches that tuyma, 2004). Hillis (2004) aptly argues that "as the Tree ofare particularlyproblematicfor it). Finally, it shows the po- Life becomes more complete, its applications are also ex-tential for morphology to be difficult to interpret and even panding exponentially.A complete Tree of Life would allowunhelpful in phylogenetic inference. At the same time, it is analyses that we would never contemplate today." He also contends that before long the phylogenetic revolution willimportant to note that the gnepines topology conflicts with have permeated the way we study all areas of biology. Therelatively few morphological characters,especially ones thatprovide a clear pattern (Burleigh and Mathews, 2004; Soltis study of the plant tree of life has, through the collaborativeet al., in press). This points to the dangerously seductive in- spirit of the field and its remarkableprogress, set the standardfluence that "charismatic singular characters,"be they mor- for tree of life efforts, and we look forward to accelerating rates of progress in the years to come.phological (Scotland et al., 2003) or "raregenomic structural"(McPherson et al., 2004), can exert compared to the numeri-cally overwhelming but unlovable mass of nucleotide se- LITERATURECITEDquence charactersthat are the foundationof virtually all well-supportedphylogenetic trees. ADAMS, K. L., Y.-L. QIu, M. STOUTEMYER, AND J. D. PALMER.2002. Punc- tuated evolution of mitochondrialgene content: high and variable rates of mitochondrial gene loss and transfer during angiosperm evolution. PROSPECTS Proceedings of the National Academy of Sciences, USA 99: 9905-9912. ALBERT, V. A. [ED.]. 2005. Parsimony, phylogeny, and genomics. Oxford With all the impressiveprogressmade over the first20 years Press, Oxford, UK, in press.or so of the DNA revolution in plant systematics, it is impor- ANDERSEN, A. 2004. Biology and systematics of heterokontand hapto- R.tant to recognize that the revolution is still at an early stage. phyte algae. American Journal of Botany 91: 1508-1522. BALDAUF, S. L., D. BHATTACHARYA, J. COCKRILL, P. HUGENHOLTZ, J. PAW-Few land plants, and even fewer algae, have been sampledfor AND A. G. B. SIMPSON.2004. The tree of life: an overview. In LOWSKI,even one gene, and fewer still for even two to four genes. J. Cracraftand M. J. 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