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Evolution: Revisiting the Root of the Eukaryote Tree

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Evolution: Revisiting the Root of the Eukaryote Tree View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by Elsevier - Publisher Connector Dispatch R165 cytokinesis and are enhanced by Rho 18. Yamada, T., Hikida, M., and Kurosaki, T. (2006). and RGA-4 in the germ line and in the early and suppressed by Rac. J. Cell Biol. 166, Regulation of cytokinesis by mgcRacGAP in B embryo of C. elegans. Development 134, 61–71. lymphocytes is independent of GAP activity. 3495–3505. 16. Severson, A.F., Baillie, D.L., and Bowerman, B. Exp. Cell Res. 312, 3517–3525. (2002). A formin homology protein and a 19. Schonegg, S., Constantinescu, A.T., Hoege, C., profilin are required for cytokinesis and and Hyman, A.A. (2007). The Rho GTPase- Department of Molecular Genetics and Cell Arp2/3-independent assembly of cortical activating proteins RGA-3 and RGA-4 are Biology, University of Chicago, Chicago, microfilaments in C. elegans. Curr. Biol. 12, required to set the initial size of PAR domains IL 60637, USA. 2066–2075. in Caenorhabditis elegans one-cell E-mail: [email protected] 17. Zhang, W., and Robinson, D.N. (2005). Balance embryos. Proc. Natl. Acad. Sci. USA of actively generated contractile and resistive 104, 14976–14981. forces controls cytokinesis dynamics. Proc. 20. Schmutz, C., Stevens, J., and Spang, A. (2007). Natl. Acad. Sci. USA 102, 7186–7191. Functions of the novel RhoGAP proteins RGA-3 DOI: 10.1016/j.cub.2008.12.028 Evolution: Revisiting the Root of the been controversial since they were first proposed [6]. Now, with the Eukaryote Tree rapid accumulation of genome-scale data for diverse protist species, a flurry of phylogenomic analyses A recent phylogenomic investigation shows that the enigmatic flagellate [7–9] are putting these hypotheses Breviata is a distinct anaerobic lineage within the eukaryote super-group to the test. Amoebozoa and challenges the unikont–bikont rooting of the tree of A recent paper by Minge et al. [7] eukaryotes. reports phylogenomic analyses of the enigmatic protist Breviata anathema, Andrew J. Roger1,2 ‘bikonts’ (all other super-groups), a small amoeba-like cell with an and Alastair G.B. Simpson1,3 as shown in Figure 1. Both the six anterior flagellum. Breviata is super-groups model and the interesting for two major reasons: it In the 1980s and 1990s, prevailing unikont–bikont root hypothesis have lives in low oxygen conditions and views of the eukaryote tree of life were strongly influenced by phylogenies of small subunit ribosomal RNA (rRNA) genes [1]. Although these analyses ‘Unikonts’ ‘Bikonts’ placed many eukaryotes into major groups, it became clear that the Archaeplastida relationships amongst these groups Apusomonads (= Plantae) could not be determined because Cryptomonads + Amoebozoa Breviata of the limited information available Haptophytes Slime moulds in a single gene, as well as Stramenopiles Archamoebae methodological artifacts [2]. More 0 Phalansterium 1 2+ recently, a ‘six super-groups’ Alveolata Multicilia hypothesis for deep eukaryote 1 1/2 2 2 2 1 2 phylogeny emerged as a synthesis of Lobose 2 Rhizaria analyses of sequence data for rRNAs, amoebae 0 2 concatenated sets of conserved 2 proteins and organellar genomes, Opisthokonts 2* Excavata and some detailed ultrastructural inc. Animals comparisons [3]. The six super-groups and Fungi proposed are the opisthokonts, Eukaryotes Amoebozoa, Archaeplastida, Prokaryotes chromalveolates, Rhizaria and Excavata. In the absence of outgroup sequences that are sufficiently Eubacteria Archaebacteria Current Biology closely related to allow reliable rooting of eukaryotes in molecular Figure 1. The placement of Breviata anathema in the eukaryote tree of life. phylogenies, Cavalier-Smith and The relationships amongst the six super-groups of eukaryotes are shown as recovered by Minge colleagues proposed that the et al. [7] and other recent phylogenomic analyses [8,9]. The hypothesized super-groups are presence or absence of colour-coded as follows: opisthokonts (purple), Amoebozoa (light blue), Archaeplastida (green), a dihidrofolate reductase-thymidylate chromalveolates (orange), Rhizaria (dark blue) and Excavata (brown). Note that recent evidence synthase (DHFR-TS) gene fusion [4] suggests that Rhizaria are specifically related to some chromalveolates [8,9]. The tree is shown and specific myosin gene families [5] as rooted according to the unikont–bikont hypothesis [5,14]. Anaerobic/microaerophilic in diverse eukaryotes could be used protistan lineages that lack classical mitochondria are shown in red. The numbers in ellipses show the inferred ancestral number of basal bodies per kinetid (flagellar unit) in the various to infer that the eukaryote root falls eukaryote lineages. The plus (+) indicates that Breviata may contain more basal bodies than between so-called ‘unikonts’ the number cited whereas the asterisk (*) indicates that one basal body is non-flagellated. (opisthokonts and Amoebozoa) and Dashed lineages indicate uncertainty in the location of that branch on the tree (see text). Current Biology Vol 19 No 4 R166 cytoskeleton and other organelles. sequence features in the small Suddenly Breviata became of key subunit rRNA genes from Breviata. interest for early eukaryote evolution: On the other hand, divergent lineages it was not assigned to any major are often placed too deep in eukaryote group, and it was just phylogenetic analyses as a result of possible that Breviata was the only long-branch attraction artifacts [2], primitively amitochondriate eukaryote and removal of rapidly-evolving lineage still alive today. ‘noisy’ sites is sometimes an Minge et al. [7] soundly refute this effective strategy for combating possibility. They conducted an this artefact. Although Minge expressed-sequence tag (EST) et al.’s [7] preference is reasonable, survey of Breviata anathema and, it will need to be tested by future from these data, constructed a data analyses with better sampling of set of 75 proteins for phylogenetic amoebozoan species. investigations. Sophisticated Even more interesting, the placement analyses indicate that Breviata is of Breviata as a basal amoebozoan most closely related to Amoebozoa, calls into question the nature of the the super-group to which the common ancestor of extant eukaryotes Archamoebae also belong. Provided implied by the unikont–bikont root the root of the eukaryotic tree falls hypothesis. Cavalier-Smith [14] Figure 2. Transmission electron micrograph elsewhere, this sister-group proposed the names ‘unikonts’ and showing the kinetid of Breviata. relationship between Breviata and the ‘bikonts’ based on a scenario for the The two arrows indicate the two basal bodies, ancestrally mitochondrion-containing evolution of the flagellar apparatus. In one of which gives rise to the flagellum (F). Amoebozoa demonstrates that most eukaryotic cells the flagellar Image kindly provided by Giselle Walker (University of Cambridge) and Aaron Heiss Breviata too descends from apparatus is the centre of organization (Dalhousie University). a mitochondrion-containing ancestor. for the cytoskeleton. Its core is usually Even more convincingly, the a single ‘kinetid’ consisting of one or authors found within their EST data more basal bodies, which may either lacks classical mitochondria; and its sequences encoding mitochondrial give rise to flagella, or be non- flagellar apparatus has at least one marker proteins such as chaperonin flagellated. Cavalier-Smith argued that additional non-flagellated basal body 60 and tim17. These findings, ancestral eukaryotes had a simple (Figure 2). Breviata was originally combined with electron kinetid with one basal body anchoring assumed to be a member of the microscopy evidence of a double one flagellum. He further suggested Archamoebae, a group of membrane-bounded organelle [13], that the ‘unikonts’ had retained this mitochondrion-lacking amoebozoans suggest that Breviata does ancestral organization, whereas the that includes organisms such as the contain some sort of relict ‘bikonts’ descended from a common human amebic dysentery parasite mitochondrion. ancestor that had evolved a kinetid with Entamoeba histolytica and the giant Anaerobic and microaerophilic two flagella, one anterior and one multinucleate amoeba Pelomyxa protists with mitochondrion-derived posterior. palustris. Archamoebae gained organelles are scattered across the In ‘bikonts’ studied to date, notoriety in the 1980s because they eukaryotic tree (Figure 1), and a vibrant a characteristic ontogenetic flagellar were widely believed to be primitive sub-field of evolutionary cell biology is transformation process occurs during eukaryotes that had diverged prior devoted to understanding how these cell division. New basal bodies always to the endosymbiotic origin of organelles evolved to function in low become the anterior units, while mitochondria [10]. The subsequent oxygen conditions [10]. Does Breviata existing basal bodies become the finding of mitochondrial represent another independent lineage posterior units in the daughter cells. marker proteins and relict of eukaryotes with modified This means that the anterior flagellum mitochondrion-derived organelles mitochondria? In Minge et al.’s [7] of the parent transforms into of unknown function in several main analysis, Breviata branches a posterior flagellum in one of the Archamoebae [11,12] proved this robustly as the sister to all other daughters. Cavalier-Smith [14] hypothesis wrong. Indeed, evidence Amoebozoa, as shown in Figure 1, suggested that the bikont kinetid for the retention of relict mitochondria implying
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