A molecular timeline for the origin of photosynthetic eukaryotes.

The appearance of photosynthetic eukaryotes (algae and plants) dramatically altered the Earth's ecosystem, making possible all vertebrate life on land, including humans. Dating algal origin is, however, frustrated by a meager fossil record. We generated a plastid multi-gene phylogeny with Bayesian inference and then used maximum likelihood molecular clock methods to estimate algal divergence times. The plastid tree was used as a surrogate for algal host evolution because of recent phylogenetic evidence supporting the vertical ancestry of the plastid in the red, green, and glaucophyte algae. Nodes in the plastid tree were constrained with six reliable fossil dates and a maximum age of 3,500 MYA based on the earliest known eubacterial fossil. Our analyses support an ancient (late Paleoproterozoic) origin of photosynthetic eukaryotes with the primary endosymbiosis that gave rise to the first alga having occurred after the split of the Plantae (i.e., red, green, and glaucophyte algae plus land plants) from the opisthokonts sometime before 1,558 MYA. The split of the red and green algae is calculated to have occurred about 1,500 MYA, and the putative single red algal secondary endosymbiosis that gave rise to the plastid in the cryptophyte, haptophyte, and stramenopile algae (chromists) occurred about 1,300 MYA. These dates, which are consistent with fossil evidence for putative marine algae (i.e., acritarchs) from the early Mesoproterozoic (1,500 MYA) and with a major eukaryotic diversification in the very late Mesoproterozoic and Neoproterozoic, provide a molecular timeline for understanding algal evolution.

[1]  Michael J. Sanderson,et al.  R8s: Inferring Absolute Rates of Molecular Evolution, Divergence times in the Absence of a Molecular Clock , 2003, Bioinform..

[2]  P. Keeling,et al.  Nucleus-Encoded, Plastid-Targeted Glyceraldehyde-3-Phosphate Dehydrogenase (GAPDH) Indicates a Single Origin for Chromalveolate Plastids , 2003 .

[3]  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.

[4]  Peter R. Crane,et al.  The origin and early evolution of plants on land , 1997, Nature.

[5]  A. Steele,et al.  Questioning the evidence for Earth's oldest fossils , 2002, Nature.

[6]  Halverson,et al.  A neoproterozoic snowball earth , 1998, Science.

[7]  A. Knoll,et al.  Proterozoic Ocean Chemistry and Evolution: A Bioinorganic Bridge? , 2002, Science.

[8]  D. Penny,et al.  Comment on "Hexapod Origins: Monophyletic or Paraphyletic?" , 2003, Science.

[9]  E. M. Friis,et al.  The origin and early diversification of angiosperms , 1995, Nature.

[10]  A. Knoll,et al.  Morphological and ecological complexity in early eukaryotic ecosystems , 2001, Nature.

[11]  J. Doyle.  Molecules, morphology, fossils, and the relationship of angiosperms and Gnetales. , 1998, Molecular phylogenetics and evolution.

[12]  L. Medlin,et al.  Phylogenetic relationships of the 'golden algae' (haptophytes, heterokont chromophytes) and their plastids , 1997 .

[13]  S. Hedges,et al.  Molecular Evidence for the Early Colonization of Land by Fungi and Plants , 2001, Science.

[14]  Michael P. Cummings,et al.  PAUP* [Phylogenetic Analysis Using Parsimony (and Other Methods)] , 2004 .

[15]  D. Cutler,et al.  Estimating divergence times in the presence of an overdispersed molecular clock. , 2000, Molecular biology and evolution.

[16]  Andrew J. Roger,et al.  A Cyanobacterial Gene in Nonphotosynthetic Protists—An Early Chloroplast Acquisition in Eukaryotes? , 2002, Current Biology.

[17]  C. Ciniglia,et al.  Comparative approaches to the taxonomy of the genus Galdieria Merola (Cyanidiales, Rhodophyta) , 2003 .

[18]  D. Penny,et al.  The root of the mammalian tree inferred from whole mitochondrial genomes. , 2003, Molecular phylogenetics and evolution.

[19]  M. P. Cummings.  PHYLIP (Phylogeny Inference Package) , 2004 .

[20]  P. Keeling,et al.  Nucleus-encoded, plastid-targeted glyceraldehyde-3-phosphate dehydrogenase (GAPDH) indicates a single origin for chromalveolate plastids. , 2003, Molecular biology and evolution.

[21]  Martin Vingron,et al.  TREE-PUZZLE: maximum likelihood phylogenetic analysis using quartets and parallel computing , 2002, Bioinform..

[22]  Michael J Benton,et al.  Dating the Tree of Life , 2003, Science.

[23]  T. Cavalier-smith.  Principles of Protein and Lipid Targeting in Secondary Symbiogenesis: Euglenoid, Dinoflagellate, and Sporozoan Plastid Origins and the Eukaryote Family Tree 1 , 2 , 1999, The Journal of eukaryotic microbiology.

[24]  Michael J. Sanderson,et al.  A Nonparametric Approach to Estimating Divergence Times in the Absence of Rate Constancy , 1997 .

[25]  J. Palmer,et al.  Evolutionary transfer of the chloroplast tufA gene to the nucleus , 1990, Nature.

[26]  W. Martin,et al.  Evolutionary analysis of 58 proteins encoded in six completely sequenced chloroplast genomes: Revised molecular estimates of two seed plant divergence times , 1997, Plant Systematics and Evolution.

[27]  W. Gillespie,et al.  The earliest seeds , 1981, Nature.

[28]  Charles F. Delwiche,et al.  The Closest Living Relatives of Land Plants , 2001, Science.

[29]  Pamela S Soltis,et al.  Rate heterogeneity among lineages of tracheophytes: Integration of molecular and fossil data and evidence for molecular living fossils , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[30]  A. Knoll,et al.  New Lu–Hf and Pb–Pb age constraints on the earliest animal fossils , 2002 .

[31]  P. Lio’,et al.  Molecular phylogenetics: state-of-the-art methods for looking into the past. , 2001, Trends in genetics : TIG.

[32]  M. V. Kranendonk,et al.  Self-Assembled Silica-Carbonate Structures and Detection of Ancient Microfossils , 2003, Science.

[33]  Debashish Bhattacharya,et al.  The single, ancient origin of chromist plastids , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[34]  J. Palmer,et al.  The origin of plastids and their spread via secondary symbiosis , 1997 .

[35]  R F Doolittle,et al.  Determining divergence times with a protein clock: update and reevaluation. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[36]  T. Wdowiak,et al.  Laser–Raman imagery of Earth's earliest fossils , 2002, Nature.

[37]  John P. Huelsenbeck,et al.  MRBAYES: Bayesian inference of phylogenetic trees , 2001, Bioinform..

[38]  S. Baldauf,et al.  The Deep Roots of Eukaryotes , 2003, Science.

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

[40]  D. Bhattacharya.  Origins of Algae and their Plastids , 1997, Plant Systematics and Evolution.

[41]  Debashish Bhattacharya,et al.  Photosynthetic eukaryotes unite: endosymbiosis connects the dots. , 2004, BioEssays : news and reviews in molecular, cellular and developmental biology.

[42]  D. Bhattacharya,et al.  PHYLOGENY OF THE BANGIOPHYCIDAE (RHODOPHYTA) AND THE SECONDARY ENDOSYMBIOTIC ORIGIN OF ALGAL PLASTIDS , 2000 .

[43]  Yuji Kohara,et al.  The Phylogenetic Position of Red Algae Revealed by Multiple Nuclear Genes from Mitochondria-Containing Eukaryotes and an Alternative Hypothesis on the Origin of Plastids , 2003, Journal of Molecular Evolution.

[44]  Debashish Bhattacharya,et al.  A single origin of the peridinin- and fucoxanthin-containing plastids in dinoflagellates through tertiary endosymbiosis , 2002, Proceedings of the National Academy of Sciences of the United States of America.

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

[46]  K. Valentin,et al.  Rubisco genes indicate a close phylogenetic relation between the plastids of Chromophyta and Rhodophyta , 1990, Plant Molecular Biology.

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

[48]  J. Felsenstein.  CONFIDENCE LIMITS ON PHYLOGENIES: AN APPROACH USING THE BOOTSTRAP , 1985, Evolution; international journal of organic evolution.

[49]  D. Gerneke,et al.  Early Archean fossil bacteria and biofilms in hydrothermally-influenced sediments from the Barberton greenstone belt, South Africa , 2001 .

[50]  D. Sankoff,et al.  Genome structure and gene content in protist mitochondrial DNAs. , 1998, Nucleic acids research.

[51]  Simon A. Wilde,et al.  Evidence from detrital zircons for the existence of continental crust and oceans on the Earth 4.4 Gyr ago , 2001, Nature.

[52]  Hervé Philippe,et al.  The origin of red algae and the evolution of chloroplasts , 2000, Nature.

[53]  David Posada,et al.  MODELTEST: testing the model of DNA substitution , 1998, Bioinform..

[54]  Sudhir Kumar,et al.  Divergence time estimates for the early history of animal phyla and the origin of plants, animals and fungi , 1999, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[55]  G. Glazko,et al.  Estimation of divergence times from multiprotein sequences for a few mammalian species and several distantly related organisms , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[56]  D. Bhattacharya,et al.  The actin gene of the glaucocystophyte Cyanophora paradoxa: analysis of the coding region and introns, and an actin phylogeny of eukaryotes , 1997, Current Genetics.

[57]  C. dePamphilis,et al.  Phylogeny of seed plants based on all three genomic compartments: extant gymnosperms are monophyletic and Gnetales' closest relatives are conifers. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[58]  T. Cavalier-smith,et al.  The neomuran origin of archaebacteria, the negibacterial root of the universal tree and bacterial megaclassification. , 2002, International journal of systematic and evolutionary microbiology.

[59]  Gabriel Gelius-Dietrich,et al.  Early Cell Evolution, Eukaryotes, Anoxia, Sulfide, Oxygen, Fungi First (?), and a Tree of Genomes Revisited , 2003, IUBMB life.

[60]  N. Butterfield.  Paleobiology of the late Mesoproterozoic (ca. 1200 Ma) Hunting Formation, Somerset Island, arctic Canada , 2001 .

[61]  T. Kuroiwa,et al.  Complete sequence and analysis of the plastid genome of the unicellular red alga Cyanidioschyzon merolae. , 2003, DNA research : an international journal for rapid publication of reports on genes and genomes.

[62]  D. Bhattacharya,et al.  THE PHYLOGENY OF PLASTIDS: A REVIEW BASED ON COMPARISONS OF SMALL‐SUBUNIT RIBOSOMAL RNA CODING REGIONS , 1995 .

[63]  A. Knoll,et al.  Three-dimensional preservation of algae and animal embryos in a Neoproterozoic phosphorite , 1998, Nature.

[64]  J. Palmer,et al.  Different fates of the chloroplast tufA gene following its transfer to the nucleus in green algae. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[65]  A. Knoll,et al.  The early evolution of eukaryotes: a geological perspective. , 1992, Science.