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Evolution: Rooting the Eukaryotic Tree of Life View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by Elsevier - Publisher Connector Dispatch R151 Dispatches Evolution: Rooting the Eukaryotic Tree of Life The root of the eukaryotic tree is a major unresolved question in evolutionary transcription and, particularly, biology. A recent study marshals mitochondrial genes to place that root translation [13]. This scenario implies between the enigmatic Excavates and all other eukaryotes, providing an that the mitochondrion was gained interesting new perspective on early eukaryotic evolution. before the radiation of all known eukaryotes, suggesting that Tom A. Williams The root of the eukaryotes has been mitochondrial genes might provide an studied intensively in recent years, interesting source of information about Eukaryotes are the group of organisms although as yet no consensus appears the eukaryotic root. The idea is that, whose cells contain a mitochondrion in sight. Published analyses have since mitochondria are descended and a nucleus. Although we often think placed the root within the Amorphea from Bacteria, trees of mitochondrial of eukaryotes as comprising animals, [7], between the Amorphea and all genes can be rooted on the bacterial plants, fungi, and the single-celled other eukaryotes [8], between the branch, polarizing the relationships protists, molecular phylogenetics has Archaeplastida (plants) and all other within the eukaryotic portion of the turned that view on its head [1]. At the eukaryotes [9], or within the Excavates tree — an approach pioneered by level of the genome, eukaryotic [10] — all with rather different Derelle and Lang [8] and developed biodiversity is largely microbial, with implications for the history and the in the recent study of He et al. [6]. each of the familiar multicellular groups process of eukaryotic evolution. While this work is unlikely to settle the arising independently from unicellular One reason for this lack of agreement debate for good, He et al. employ ancestors [2]. In this emerging view, may be the intrinsic difficulty of rooting state-of-the-art methods, and their which is based mainly on phylogenetic the eukaryotic tree. The great analyses focus attention on the most analyses of large sets of broadly evolutionary distance that separates important challenges remaining in this distributed genes [3–5], most eukaryotes from their closest field. eukaryotes can be classified into one of prokaryotic relatives makes standard As a starting point for their analyses, three major lineages. These are the phylogenetic rooting approaches He et al. [6] screened genomes from Amorphea (animals, fungi, and unreliable and prone to artefact. This the Amorphea, Diaphoretickes and Amoebozoans such as the slime mould has led authors to explore alternative Excavates for mitochondrial genes. Dictyostelium), the Diaphoretickes approaches, such as using the They identified 37 genes which were (including plants and most other information from gene duplications and found in all, or almost all, eukaryotes, photosynthetic eukaryotes), and the losses [7] or slowly evolving molecular and whose closest prokaryotic Excavates — a diverse group of characters such as gene fusions [9] to homologues were among the Bacteria. unicellular eukaryotes that includes root the tree. The problem is that when They found that the protein products important parasites such as Giardia, these alternative strategies disagree, of most of these genes were targeted Trichomonas, and Trypanosoma. it is difficult to determine the best to the mitochondria of modern Despite this rapid progress, some of approach. As an added difficulty, the eukaryotes, consistent with the idea the most interesting questions about interior branches of the eukaryotic tree that the genes originally entered the eukaryotic evolution remain separating the major groups often eukaryotic lineage with the ancestor of unresolved. Foremost among these appear to be rather short, perhaps the mitochondrion. Note that these is the position of the root of the suggesting that the Amorphea, genes are often not encoded by the eukaryotic tree, a critical point Diaphoretickes and Excavates mitochondrial genome, because many about which there is currently little diverged from each other over a mitochondrial genes have been consensus. A new study by He et al. [6] relatively short period of time following transferred to the nucleus during reported in this issue of Current Biology the origin of eukaryotes — the eukaryotic evolution [14]. Importantly, represents an important contribution to so-called ‘big bang’ of eukaryotic He et al. were able to show that their this ongoing debate. evolution [11,12]. set of genes contained a consistent The root of a phylogenetic tree Despite these difficulties in inferring phylogenetic signal within the is fundamental to its biological the root, recent discoveries have eukaryotes — that is, that they interpretation, defining the starting fleshed out our understanding of generally agreed on the structure of the point and polarizing the subsequent eukaryotic origins and the ancestral eukaryotic tree. Since each gene on its divergence events within the tree. For eukaryote. The balance of evidence own did not provide much rooting the eukaryotic tree, the root position is now favours a symbiogenic origin for information, the authors combined all critical for identifying the genes and the eukaryotic cell, in which an 37 genes and inferred a single tree. traits that may have been present in the Alpha-proteobacterium — the ancestor Assuming that the mitochondrion was ancestral eukaryote, for tracing the of the mitochondrion — formed a acquired before the diversification of evolution of these traits throughout partnership with an Archaeon, the main eukaryotic lineages, this tree the eukaryotic radiation, and for whose trace in modern eukaryotes could then be rooted on the branch establishing the deep relationships is found mainly in the genetic leading to the bacterial outgroups among the major eukaryotic groups. apparatus of DNA synthesis, (Figure 1). Following this logic, He et al. Current Biology Vol 24 No 4 R152 Excavates have much to learn about the earliest period of eukaryotic evolution, and will surely stimulate further debate. References Mitochondrion 1. Adl, S.M., Simpson, A.G.B., Lane, C.E., Lukes, J., Bass, D., Bowser, S.S., Brown, M.W., Burki, F., Dunthorn, M., Hampl, V., et al. (2012). mtDNA mtDNA The revised classification of eukaryotes. Diaphoretickes J. Eukaryot. Microbiol. 59, 429–493. 2. O’Malley, M.A., Simpson, A.G.B., and Alpha-proteobacterium Roger, A.J. (2012). The other eukaryotes in light Ancestral eukaryote of evolutionary protistology. Biol. Philos. 28, 299–330. 3. Parfrey, L.W., Grant, J., Tekle, Y.I., Lasek- Nesselquist, E., Morrison, H.G., Sogin, M.L., Amorphea Patterson, D.J., and Katz, L.A. (2010). Broadly sampled multigene analyses yield a Current Biology well-resolved eukaryotic tree of life. Syst. Biol. 59, 518–533. 4. Burki, F., Shalchian-Tabrizi,K., and Pawlowski, J. Figure 1. Mitochondrial genes root the eukaryotic tree. (2008). Phylogenomics reveals a new ‘megagroup’ including most photosynthetic Genes that entered the eukaryotic lineage with the mitochondrial endosymbiont trace the sub- eukaryotes. Biol. Lett. 4, 366–369. sequent evolutionary diversification of the eukaryotes. The recent study of He et al. [6] sug- 5. Hampl, V., Hug, L., Leigh, J.W., Dacks, J.B., gests that one of the deepest splits lies between the Excavates and all other eukaryotes. Lang, B.F., Simpson, A.G.B., and Roger, A.J. (2009). Phylogenomic analyses support the monophyly of Excavata and resolve rooted the tree between the Excavates comes down to the definition of relationships among eukaryotic ‘supergroups’. Proc. Natl. Acad. Sci. USA 106, 3859–3864. and all other eukaryotes. mitochondrial genes: while He et al. 6. He, D., Fiz-Palacios, O., Fu, C.-J., Fehling, J., If correct, an Excavate root would emphasised bacterial genes that Tsai, C.-C., and Baldauf, S.L. (2014). An reinforce the astonishing biodiversity of contain a congruent phylogenetic alternative root for the eukaryotic tree of life. Curr. Biol. 24, 465–470. microbial eukaryotes by placing all of signal and are broadly conserved 7. Katz, L.A., Grant, J.R., Parfrey, L.W., and the familiar multicellular groups — across eukaryotes, Derelle and Lang Burleigh, J.G. (2012). Turning the crown upside down: gene tree parsimony roots the animals, plants, and fungi — on one screened for eukaryotic genes of eukaryotic tree of life. Syst. Biol. 61, 653–660. side of the eukaryotic tree. It would also alpha-proteobacterial affinity, based 8. Derelle, R., and Lang, B.F. (2012). Rooting the support an emerging view of the last on the idea that the mitochondrion eukaryotic tree with mitochondrial and bacterial proteins. Mol. Biol. Evol. 29, common eukaryotic ancestor as a is descended from an Alpha- 1277–1289. relatively complex single-celled proteobacterium. As a result of these 9. Rogozin, I.B., Basu, M.K., Csu¨ro¨ s, M., and Koonin, E.V. (2009). Analysis of rare genomic organism that already possessed a different criteria, there was only changes does not support the unikont-bikont gene repertoire comparable in size moderate overlap between the genes phylogeny and suggests cyanobacterial and complexity to modern used in the two studies. In particular, symbiosis as the point of primary radiation of eukaryotes. Genome Biol. Evol. 1, 99–113. eukaryotes [15,16]. not all of the genes analyzed by He et al. 10. Cavalier-Smith, T. (2010). Kingdoms Protozoa But with a number of incompatible are alpha-proteobacterial, with some and Chromista and the eozoan root of the eukaryotic tree. Biol. Lett. 6, 342–345. rootings now proposed for the tracing their ancestry to other bacterial 11. Koonin, E.V. (2010). The origin and early eukaryotic tree, why should this new groups. This does not necessarily rule evolution of eukaryotes in the light of root be preferred to any of the out a mitochondrial origin, because the phylogenomics. Genome Biol. 11, 209. 12. Eme, L., Sharpe, S.C., Brown, M.W., and alternatives? One reason might be the ancestral mitochondrial genome likely Roger, A.J.
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