The tree of eukaryotes.

Recent advances in resolving the tree of eukaryotes are converging on a model composed of a few large hypothetical 'supergroups', each comprising a diversity of primarily microbial eukaryotes (protists, or protozoa and algae). The process of resolving the tree involves the synthesis of many kinds of data, including single-gene trees, multigene analyses, and other kinds of molecular and structural characters. Here, we review the recent progress in assembling the tree of eukaryotes, describing the major evidence for each supergroup, and where gaps in our knowledge remain. We also consider other factors emerging from phylogenetic analyses and comparative genomics, in particular lateral gene transfer, and whether such factors confound our understanding of the eukaryotic tree.

[1]  C. Kurland Something for everyone , 2000, EMBO reports.

[2]  C. Kurland,et al.  Horizontal gene transfer: A critical view , 2003 .

[3]  A. Simpson,et al.  Cytoskeletal organization, phylogenetic affinities and systematics in the contentious taxon Excavata (Eukaryota). , 2003, International journal of systematic and evolutionary microbiology.

[4]  N. Butterfield,et al.  Bangiomorpha pubescens n. gen., n. sp.: implications for the evolution of sex, multicellularity, and the Mesoproterozoic/Neoproterozoic radiation of eukaryotes , 2000, Paleobiology.

[5]  A. Simpson,et al.  Eukaryotic Evolution: Getting to the Root of the Problem , 2002, Current Biology.

[6]  O. Gascuel Mathematics of Evolution & Phylogeny , 2005 .

[7]  C. Berney,et al.  Small-subunit ribosomal RNA gene sequences of Phaeodarea challenge the monophyly of Haeckel's Radiolaria. , 2004, Protist.

[8]  P. Keeling,et al.  On the monophyly of chromalveolates using a six-protein phylogeny of eukaryotes. , 2005, International journal of systematic and evolutionary microbiology.

[9]  P. Holland,et al.  Phylogenomics of eukaryotes: impact of missing data on large alignments. , 2004, Molecular biology and evolution.

[10]  H. Ochman,et al.  Lateral gene transfer and the nature of bacterial innovation , 2000, Nature.

[11]  J A Eisen,et al.  Microbial Genes in the Human Genome: Lateral Transfer or Gene Loss? , 2001, Science.

[12]  F. Delsuc,et al.  The timing of eukaryotic evolution: does a relaxed molecular clock reconcile proteins and fossils? , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[13]  T. Cavalier-smith,et al.  The root of the eukaryote tree pinpointed , 2003, Current Biology.

[14]  Yves Van de Peer,et al.  Evolutionary Relationships Among the Eukaryotic Crown Taxa Taking into Account Site-to-Site Rate Variation in 18S rRNA , 1997, Journal of Molecular Evolution.

[15]  J. Huelsenbeck,et al.  Bayesian phylogenetic analysis of combined data. , 2004, Systematic biology.

[16]  G. H. Coombs,et al.  Evolutionary relationships among protozoa. , 1998 .

[17]  S. Stickel,et al.  Monophyletic origins of the metazoa: an evolutionary link with fungi , 1993, Science.

[18]  B Franz Lang,et al.  Mitochondria of protists. , 2004, Annual review of genetics.

[19]  W. Doolittle,et al.  A kingdom-level phylogeny of eukaryotes based on combined protein data. , 2000, Science.

[20]  A. Simpson,et al.  On Core Jakobids and Excavate Taxa: The Ultrastructure of Jakoba incarcerata , 2001, The Journal of eukaryotic microbiology.

[21]  H. Phillipe The molecular phylogeny of eukaryota: solid facts and uncertainties , 1998 .

[22]  W. Doolittle,et al.  How big is the iceberg of which organellar genes in nuclear genomes are but the tip? , 2003, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[23]  P. Thier,et al.  The origin of red algae and the evolution of chloroplasts , 2022 .

[24]  P. Keeling,et al.  Foraminifera and Cercozoa share a common origin according to RNA polymerase II phylogenies. , 2003, International journal of systematic and evolutionary microbiology.

[25]  N. Patron,et al.  Gene Replacement of Fructose-1,6-Bisphosphate Aldolase Supports the Hypothesis of a Single Photosynthetic Ancestor of Chromalveolates , 2004, Eukaryotic Cell.

[26]  N. Galtier,et al.  Maximum-likelihood phylogenetic analysis under a covarion-like model. , 2001, Molecular biology and evolution.

[27]  T. Cavalier-smith Protist phylogeny and the high-level classification of Protozoa , 2003 .

[28]  B F Lang,et al.  Complete Sequence of the Mitochondrial DNA of the Red Alga Porphyra purpurea: Cyanobacterial Introns and Shared Ancestry of Red and Green Algae , 1999, Plant Cell.

[29]  O. Bininda-Emonds,et al.  The evolution of supertrees. , 2004, Trends in ecology & evolution.

[30]  W. Doolittle,et al.  Alpha-tubulin from early-diverging eukaryotic lineages and the evolution of the tubulin family. , 1996, Molecular biology and evolution.

[31]  Debashish Bhattacharya,et al.  A molecular timeline for the origin of photosynthetic eukaryotes. , 2004, Molecular biology and evolution.

[32]  Mike Steel,et al.  Should phylogenetic models be trying to "fit an elephant"? , 2005, Trends in genetics : TIG.

[33]  J. Palmer,et al.  Investigating Deep Phylogenetic Relationships among Cyanobacteria and Plastids by Small Subunit rRNA Sequence Analysis 1 , 1999, The Journal of eukaryotic microbiology.

[34]  D. Roos,et al.  Nuclear-encoded, plastid-targeted genes suggest a single common origin for apicomplexan and dinoflagellate plastids. , 2001, Molecular biology and evolution.

[35]  M. Sogin,et al.  A mitochondrial-like chaperonin 60 gene in Giardia lamblia: evidence that diplomonads once harbored an endosymbiont related to the progenitor of mitochondria. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[36]  B. Lang,et al.  The Closest Unicellular Relatives of Animals , 2002, Current Biology.

[37]  N. B. Petrov,et al.  The twilight of Heliozoa and rise of Rhizaria, an emerging supergroup of amoeboid eukaryotes. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[38]  J. Andersson,et al.  Lateral gene transfer in eukaryotes , 2005, Cellular and Molecular Life Sciences CMLS.

[39]  Masami Hasegawa,et al.  Root of the Eukaryota tree as inferred from combined maximum likelihood analyses of multiple molecular sequence data. , 2005, Molecular biology and evolution.

[40]  Jeffrey D. Palmer,et al.  Widespread horizontal transfer of mitochondrial genes in flowering plants , 2003, Nature.

[41]  W. Doolittle,et al.  Lateral genomics. , 1999, Trends in cell biology.

[42]  N. Butterfield Probable Proterozoic fungi , 2005, Paleobiology.

[43]  P. Keeling,et al.  Bacterial Catalase in the Microsporidian Nosema locustae: Implications for Microsporidian Metabolism and Genome Evolution , 2003, Eukaryotic Cell.

[44]  P. Keeling Foraminifera and Cercozoa are related in actin phylogeny: two orphans find a home? , 2001, Molecular biology and evolution.

[45]  F. Delsuc,et al.  Phylogenomics and the reconstruction of the tree of life , 2005, Nature Reviews Genetics.

[46]  Yuji Inagaki,et al.  A class of eukaryotic GTPase with a punctate distribution suggesting multiple functional replacements of translation elongation factor 1alpha. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[47]  Patricia J. Johnson,et al.  Ancient Invasions: From Endosymbionts to Organelles , 2004, Science.

[48]  Elchanan Mossel,et al.  How much can evolved characters tell us about the tree that generated them? , 2004, Mathematics of Evolution and Phylogeny.

[49]  Miklós Müller,et al.  Mitochondrial remnant organelles of Giardia function in iron-sulphur protein maturation , 2003, Nature.

[50]  P. Keeling,et al.  Re-examining Alveolate Evolution Using Multiple Protein Molecular Phylogenies , 2002, The Journal of eukaryotic microbiology.

[51]  P. Keeling,et al.  Lateral gene transfer and the evolution of plastid-targeted proteins in the secondary plastid-containing alga Bigelowiella natans , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[52]  Naiara Rodríguez-Ezpeleta,et al.  Monophyly of Primary Photosynthetic Eukaryotes: Green Plants, Red Algae, and Glaucophytes , 2005, Current Biology.

[53]  J. Lake,et al.  Horizontal gene transfer among genomes: the complexity hypothesis. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[54]  Detlef D. Leipe,et al.  Evolutionary history of "early-diverging" eukaryotes: the excavate taxon Carpediemonas is a close relative of Giardia. , 2002, Molecular biology and evolution.

[55]  C. Kurland,et al.  What tangled web: barriers to rampant horizontal gene transfer. , 2005, BioEssays : news and reviews in molecular, cellular and developmental biology.

[56]  P. Keeling,et al.  A novel polyubiquitin structure in Cercozoa and Foraminifera: evidence for a new eukaryotic supergroup. , 2003, Molecular biology and evolution.

[57]  T. Cavalier-smith,et al.  Rooting the Eukaryote Tree by Using a Derived Gene Fusion , 2002, Science.

[58]  Sabine Cornelsen,et al.  Evolutionary analysis of Arabidopsis, cyanobacterial, and chloroplast genomes reveals plastid phylogeny and thousands of cyanobacterial genes in the nucleus , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[59]  T. Cavalier-smith The phagotrophic origin of eukaryotes and phylogenetic classification of Protozoa. , 2002, International journal of systematic and evolutionary microbiology.

[60]  D. Bhattacharya,et al.  Comparative Analysis of the Complete Plastid Genome Sequence of the Red Alga Gracilaria tenuistipitata var. liui Provides Insights into the Evolution of Rhodoplasts and Their Relationship to Other Plastids , 2004, Journal of Molecular Evolution.

[61]  P. J. Johnson,et al.  A common evolutionary origin for mitochondria and hydrogenosomes. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[62]  W. Doolittle,et al.  Origin and evolution of the slime molds (Mycetozoa) , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[63]  D. Graur,et al.  Reading the entrails of chickens: molecular timescales of evolution and the illusion of precision. , 2004, Trends in genetics : TIG.

[64]  Lindell Bromham,et al.  Molecular dating when rates vary. , 2005, Trends in ecology & evolution.

[65]  T. Cavalier-smith A 6-Klngdom Classification And A Unified Phylogeny , 1983 .

[66]  A. Knoll,et al.  TEM evidence for eukaryotic diversity in mid‐Proterozoic oceans , 2004 .

[67]  Andrew J. Roger,et al.  Reconstructing Early Events in Eukaryotic Evolution , 1999, The American Naturalist.

[68]  J. Palmer,et al.  Animals and fungi are each other's closest relatives: congruent evidence from multiple proteins. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[69]  T. Embley,et al.  Horizontal gene transfer and the evolution of parasitic protozoa. , 2003, Protist.

[70]  Mitchell L Sogin Early evolution and the origin of eukaryotes , 1992, Current Biology.

[71]  S Blair Hedges,et al.  BMC Evolutionary Biology BioMed Central , 2003 .

[72]  J. Eisen Horizontal gene transfer among microbial genomes: new insights from complete genome analysis. , 2000, Current opinion in genetics & development.

[73]  M. Gouy,et al.  Early origin of foraminifera suggested by SSU rRNA gene sequences. , 1996, Molecular biology and evolution.

[74]  J. Andersson,et al.  Phylogenetic Analyses of Diplomonad Genes Reveal Frequent Lateral Gene Transfers Affecting Eukaryotes , 2003, Current Biology.

[75]  J. McInerney,et al.  The Opisthokonta and the Ecdysozoa may not be clades: stronger support for the grouping of plant and animal than for animal and fungi and stronger support for the Coelomata than Ecdysozoa. , 2005, Molecular biology and evolution.

[76]  S. Porter PORTER – EARLY EUKARYOTIC DIVERSIFICATION 35 THE FOSSIL RECORD OF EARLY EUKARYOTIC DIVERSIFICATION , 2004 .

[77]  Bernard B. Suh,et al.  The genome of the protist parasite Entamoeba histolytica , 2005, Nature.

[78]  Terry Gaasterland,et al.  The analysis of 100 genes supports the grouping of three highly divergent amoebae: Dictyostelium, Entamoeba, and Mastigamoeba , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[79]  T. Cavalier-smith,et al.  A revised six‐kingdom system of life , 1998, Biological reviews of the Cambridge Philosophical Society.