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Eukaryotic Evolution: Getting to the Dispatch Root of the Problem

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Eukaryotic Evolution: Getting to the Dispatch Root of the Problem View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by Elsevier - Publisher Connector Current Biology, Vol. 12, R691–R693, October 15, 2002, ©2002 Elsevier Science Ltd. All rights reserved. PII S0960-9822(02)01207-1 Eukaryotic Evolution: Getting to the Dispatch Root of the Problem Alastair G.B. Simpson and Andrew J. Roger diatoms), cryptomonads and probably haptophyte algae. A major grouping of flagellates and amoebae, the ‘cercozoa’, emerged from improved taxon sampling of Comparative analyses of multiple genes suggest small subunit rRNAs. Recent evidence indicates that most known eukaryotes can be classified into half a the Foraminifera, and perhaps the Radiolaria, may dozen ‘super-groups’. A new investigation of the dis- belong with this assemblage [5–7]. Most ‘typical’ tribution of a fused gene pair amongst these ‘super- amoebae (such as Amoeba and Acanthamoeba), myce- groups’ has greatly narrowed the possible positions tozoan slime moulds, and the mitochondrion-lacking of the root of the eukaryote tree, clarifying the broad pelobionts and entamoebae form the ‘amoebozoa’. outlines of early eukaryote evolution. Most controversially, morphological data suggest a grouping, the ‘excavates’, which includes diplomonads and parabasalids (previously thought to be early- A decade ago, phylogenies based on small subunit diverging) together with Euglenozoa, Heterolobosea, ribosomal (r)RNA sequences provided an intuitively jakobids and several other protists [8]. appealing evolutionary tree of eukaryotes. Complex But where does the root lie? Philippe et al. [2] noted eukaryotes, including animals, fungi, plants and most that land plants (plantae), alveolates (chromalveolates) algae, emerged as a broad radiation usually called and some Euglenozoa (excavates) have fused genes the ‘eukaryotic crown’ [1]. Below this ‘crown’, more encoding a protein with both dihydrofolate reductase bizarre, and generally simpler, organisms diverged in a (DHFR) and thymidylate synthase (TS) activities. In ladder-like succession. The small subunit rRNA tree animals and fungi, these genes encode separate was ‘rooted’ with mitochondrion-lacking unicellular proteins, as in prokaryotes. Might this gene fusion be a eukaryotes such as diplomonads, parabasalids and derived feature within eukaryotes? This possibility microsporidia forming the basal branches (Figure 1a). prompted Stechmann and Cavalier-Smith [3] to examine But several studies now indicate that this rooting other groups for evidence of fused DHFR–TS. They was patterned more by methodological artefact than determined partial sequences of fused DHFR–TS genes historical signal, temporarily encouraging a view of in two chromalveolates (a stramenopile and a ciliate), eukaryote phylogeny as a large unresolved radiation [2]. another euglenozoan, and, most interestingly, a cerco- Recent years have seen tremendous progress in zoan plus two unplaced unicellular heterotrophs — an resolving this ‘radiation’. A wealth of single and apusomonad, and a centrohelid heliozoan. Apparently, concatenated gene phylogenies, improved taxon just two of the six super-groups may lack the gene sampling and examination of strong shared-derived fusion — the opisthokonts and amoebozoa. characters have revealed several novel eukaryote Under the simplest interpretation, the DHFR–TS ‘super-groups’. The hardest question of all — the fusion character drastically reduces the possible placement of the root in the eukaryote tree — has now locations for the eukaryote root. Stechmann and been clarified by Stechmann and Cavalier-Smith’s [3] Cavalier-Smith [3] argue that just three clusters need work on the phylogenetic distribution of a gene fusion consideration: opisthokonts, amoebozoa and the in eukaryotes. ‘fusion-bearing cluster’ of plantae, chromalveolates, Most known eukaryotes seem to fall into six ‘super- cercozoa (with Foraminifera and Radiolaria) and exca- groups’. The longest recognised super-group is the vates. Of these, only amoebozoa could ‘include’ the ‘opisthokonts’, including animals, fungi and a variety of root, because of the putatively derived nature of the unicellular relatives. As reported by Lang et al. [4] in this DHFR–TS fusion, and the opisthokont-specific EF-1α issue, the relationships within the opisthokonts — sequence insertion (see Figure 1 legend). Stechmann specifically the identification of the protistan sisters of and Cavalier-Smith [3] tentatively favour a rooting animals — have now been addressed by concatenated between amoebozoa plus the fusion cluster on one mitochondrial protein phylogenies. The ‘plantae’ side, and the opisthokonts alone on the other. This includes land plants and green algae, as well as red would place animals, fungi and their relatives in the algae and the obscure glaucocystophyte algae. Most ‘basal’ position in the eukaroytic tree: a humbling other eukaryote algae, and many heterotrophs, belong reversal for humans when compared to our previous to the ‘chromalveolate’ assemblage, which unites alve- lofty ‘crown’ position under the small subunit rRNA- olates (dinoflagellates, ciliates, Apicomplexa), stra- based model. menopiles/heterokonts (including brown algae and The DHFR–TS fusion provides the best estimate to date for the placement of the eukaryotic root. The Canadian Institute for Advanced Research, Program in DHFR–TS story could be misleading, however, if fused Evolutionary Biology, Genome Atlantic, Department of genes were acquired more than once in eukaryotic Biochemistry and Molecular Biology, Dalhousie University, evolution, either by multiple fusion events, or by Halifax, Nova Scotia B3H 4H7, Canada. eukaryote-to-eukaryote lateral gene transfers and E-mail: [email protected] and replacements. Alternatively the fused gene may be [email protected] ancestral for extant eukaryotes, with the separated Dispatch R692 A Eukaryote tree, B Eukaryote tree, circa 1993 2002 Cercozoa "Fusion (w/ Foraminifera, cluster" Diplomonads, w/ Radiolaria??) "Eukaryotic Retortamonads, crown" Carpediemonas, Plants + Plantae Excavates Parabasalia Green algae Stramenopiles, Animals Euglenozoa, Red algae Alveolates, Heterolobosea Glaucocystophytes Red algae, Fungi Malawimonas Chrom- etc. Plants Amoebozoa Oxymonads, Alveolates alveolates Trimastix Cryptophytes Euglenozoa, "Typical" amoebae Jakobids Stramenopiles Heterolobosea, ? Haptophytes Entamoebae, Mycetozoan slime moulds ? Mycetozoa, Pelobionts + Entamoebae Centrohelid Heliozoa Various amoebae Animals Apusomonads Parabasalia Choanoflagellates Diplomonads Mitochondria Ichthyosporea DHFR-TS fusion Microsporidia Fungi (w/ microsporidia) Nucleariid amoebae Others: Eukaryotic Mitochondria Eukaryotic Phalansterium Opisthokonts root Collodictyonids root Spironemids Eukaryotes Eukaryotes Kathablepharids Prokaryotes Telonema Prokaryotes Stephanopogon Multicilia etc. Eubacteria Archaea ArchaeaEubacteria Current Biology Figure 1. Contrasting views of eukaryotic evolution. (A) Eukaryotic evolution, as understood circa 1993 from small subunit ribosomal RNA phylogenies (after [1]). The earliest divergences involve amitochondriate protists, with animals ‘remote’ from the root. (B) Current view of eukaryotic phylogeny, with super-groups as determined primarily by multiple gene phylogenies, and with the deepest structure resolved according to the simplest interpretation of the DHFR–TS fusion, as reported by Stechmann and Cavalier-Smith [3]. Opisthokonts (purple), including animals and Fungi are sup- ported by multiple gene phylogenies, and a large insertion in EF1α (see [13,14]). Relationships with opisthokonts are resolved as in [4]. Amoebozoa (light blue) include mycetozoan slime moulds, which are allied to typical amoebae (Euamoebae) by actin trees and a cox1–cox2 gene fusion [2,9], and to amitochondriate pelobionts and entamoebae in large concatenated gene trees [15]. Plantae, includ- ing land plants, are united, somewhat weakly, by concatenated gene phylogenies [16]. Chromalveolates (excluding haptophytes) are weakly grouped by concatenated protein phylogenies [14,15], but share a gene replacement of plastid GAPDH by a nuclear-derived copy, implying a common origin of their secondary plastids, where present [17]. Inclusion of haptophytes is widely expected, but not yet demonstrated [18]. Cercozoa are placed together and ‘adjacent to’ Radiolaria in small subunit ribosomal RNA phylogenies [6,7,18]. Some small subunit rRNA trees weakly place Radiolaria in an exclusive group with cercozoa (A.G.B.S., unpublished data). Actin trees imply a cercozoan-formaniferan relationship [5]. Within excavates, diplomonads plus parabasalids and Euglenozoa plus Heterolobosea groupings are recovered in several gene trees [14,19]. All excavates except parabasalids and Euglenozoa share a suite of cytoskeletal similarities, but almost never form a single group in molecular trees [8,9,14,20]. Apusomonads and centrohelid heliozoa have the DHFR–TS gene fusion [3], but no strong evidence suggests that they fall with any particular super-group. Some other taxa with con- temporary identities, but no robust position in tree are listed under ‘others’. Branch lengths are arbitrary, and all multifircations repre- sent uncertainty as to branching order. Branches currently lacking molecular corroboration are indicated with question marks. genes in opisthokonts being the derived condition. conflict with other examinations of similar datasets This ‘reversal’ could arise if multiple copies of the [8,9]. Certain excavates, the jakobids,
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