Phylogenetic relationships among algae based on complete large-subunit rRNA sequences.

The complete or nearly complete large-subunit rRNA (LSU rRNA) sequences were determined for representatives of several algal groups such as the chlorarachniophytes, cryptomonads, haptophytes, bacillariophytes, dictyochophytes and pelagophytes. Our aim was to study the phylogenetic position and relationships of the different groups of algae, and in particular to study the relationships among the different classes of heterokont algae. In LSU rRNA phylogenies, the chlorarachniophytes, cryptomonads and haptophytes seem to form independent evolutionary lineages, for which a specific relationship with any of the other eukaryotic taxa cannot be demonstrated. This is in accordance with phylogenies inferred on the basis of the small-subunit rRNA (SSU rRNA). Regarding the heterokont algae, which form a well-supported monophyletic lineage on the basis of LSU rRNA, resolution between the different classes could be improved by combining the SSU and LSU rRNA data. Based on a concatenated alignment of both molecules, the phaeophytes and the xanthophytes are sister taxa, as well as the pelagophytes and the dictyochophytes, and the chrysophytes and the eustigmatophytes. All these sister group relationships are highly supported by bootstrap analysis and by different methods of tree construction.

[1]  S. P. Gibbs THE CHLOROPLASTS OF SOME ALGAL GROUPS MAY HAVE EVOLVED FROM ENDOSYMBIOTIC EUKARYOTIC ALGAE , 1981, Annals of the New York Academy of Sciences.

[2]  R. Wetherbee,et al.  A PHYLOGENETIC ANALYSIS OF THE SYNUROPHYCEAE USING MOLECULAR DATA AND SCALE CASE MORPHOLOGY , 1997 .

[3]  S. P. Gibbs The evolution of algal chloroplasts , 1992 .

[4]  T. Cavalier-smith,et al.  Diversification of a Chimaeric Algal Group, the Chlorarachniophytes: Phylogeny of Nuclear and Nucleomorph Small-Subunit rRNA Genes , 1999 .

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

[6]  T. Cavalier-smith,et al.  Ribosomal RNA Evidence for Chloroplast Loss within Heterokonta: Pedinellid Relationships and a Revised Classification of Ochristan Algae , 1995 .

[7]  R. Andersen,et al.  Phylogenetic analyses of the rbcL sequences from haptophytes and heterokont algae suggest their chloroplasts are unrelated. , 1997, Molecular biology and evolution.

[8]  R. Gutell,et al.  Are red algae plants , 1995 .

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

[10]  Charles F. Delwiche,et al.  Tracing the Thread of Plastid Diversity through the Tapestry of Life , 1999, The American Naturalist.

[11]  R. Andersen SYNUROPHYCEAE CLASSIS NOV., A NEW CLASS OF ALGAE , 1987 .

[12]  J. M. Whatley Membranes and Plastid Origins , 1992 .

[13]  M. Hasegawa,et al.  Gene transfer to the nucleus and the evolution of chloroplasts , 1998, Nature.

[14]  C. Woese,et al.  Ribosomal RNA sequence suggests microsporidia are extremely ancient eukaryotes , 1987, Nature.

[15]  David M. Williams PHYLOGENETIC RELATIONSHIPS AMONG THE CHROMISTA: A REVIEW AND PRELIMINARY ANALYSIS , 1991, Cladistics : the international journal of the Willi Hennig Society.

[16]  M. Sogin,et al.  Ribosomal RNA sequences of Sarcocystis muris, Theileria annulata and Crypthecodinium cohnii reveal evolutionary relationships among apicomplexans, dinoflagellates, and ciliates. , 1991, Molecular and biochemical parasitology.

[17]  M. Melkonian,et al.  Comparisons of nuclear-encoded small-subunit ribosomal RNAs reveal the evolutionary position of the Glaucocystophyta. , 1995, Molecular biology and evolution.

[18]  W. Doolittle,et al.  Microsporidia are related to Fungi: evidence from the largest subunit of RNA polymerase II and other proteins. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[19]  R. Andersen,et al.  ULTRASTRUCTURE AND 18S RRNA GENE SEQUENCE FOR PELAGOMONAS CALCEOLATA GEN. ET SP. NOV. AND THE DESCRIPTION OF A NEW ALGAL CLASS, THE PELAGOPHYCEAE CLASSIS NOV. 1 , 1993 .

[20]  T. Cavalier-smith The Origin, Losses and Gains of Chloroplasts , 1992 .

[21]  R. Bidigare,et al.  Phaeothamniophyceae Classis Nova: A New Lineage of Chromophytes Based upon Photosynthetic Pigments, rbcL Sequence Analysis and Ultrastructure. , 1998, Protist.

[22]  D. Hibberd,et al.  Observations on the Cytology and Ultrastructure of the New Algal Class, Eustigmatophyceae , 1972 .

[23]  D. M. Williams Cladistic methods and chromophyte phylogeny. , 1991, Bio Systems.

[24]  D. Bhattacharya,et al.  ALGAE CONTAINING CHLOROPHYLLS a + c ARE PARAPHYLETIC: MOLECULAR EVOLUTIONARY ANALYSIS OF THE CHROMOPHYTA , 1992, Evolution; international journal of organic evolution.

[25]  M. Melkonian,et al.  Molecular Evolutionary Analyses of Nuclear‐Encoded Small Subunit Ribosomal RNA Identify an Independent Rhizopod Lineage Containing the Euglyphina and the Chlorarachniophyta , 1995, The Journal of eukaryotic microbiology.

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

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

[28]  P. D. Rijk,et al.  The phylogeny of the Hyphochytriomycota as deduced from ribosomal RNA sequences of Hyphochytrium catenoides. , 1995 .

[29]  R. Andersen,et al.  Cladistic analyses of combined traditional and molecular data sets reveal an algal lineage. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[30]  D. Patterson Stramenopiles: Chromophytes from a protistan perspective , 1989 .

[31]  W. Ford Doolittle,et al.  An Updated and Comprehensive rRNA Phylogeny of (Crown) Eukaryotes Based on Rate-Calibrated Evolutionary Distances , 2000, Journal of Molecular Evolution.

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

[33]  G. McFadden Second-hand Chloroplasts: Evolution of Cryptomonad Algae , 1993 .

[34]  P. de Rijk,et al.  The origin of red algae and cryptomonad nucleomorphs: A comparative phylogeny based on small and large subunit rRNA sequences of Palmaria palmata, Gracilaria verrucosa, and the Guillardia theta nucleomorph. , 1998, Molecular phylogenetics and evolution.

[35]  Y. Peer,et al.  Microsporidia: accumulating molecular evidence that a group of amitochondriate and suspectedly primitive eukaryotes are just curious fungi. , 2000, Gene.

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

[37]  M. Sogin,et al.  Sequence Analysis of the Small Subunit Ribosomal Rnas of Three Zoosporic Fungi and Implications for Fungal Evolution , 1990 .

[38]  S. Baldauf A Search for the Origins of Animals and Fungi: Comparing and Combining Molecular Data , 1999, The American Naturalist.

[39]  Yves Van de Peer,et al.  The European Large Subunit Ribosomal RNA database , 2000, Nucleic Acids Res..

[40]  R. de Wachter,et al.  Complete large subunit ribosomal RNA sequences from the heterokont algae Ochromonas danica, Nannochloropsis salina, and Tribonema aequale, and phylogenetic analysis. , 1997, Journal of molecular evolution.

[41]  Y. van de Peer,et al.  Phylogenetic analysis of the SSU rRNA from members of the Chrysophyceae. , 1999, Protist.

[42]  M. Sogin,et al.  Eukaryote origins and protistan diversity. The origin and evolution of prokaryotic and eukaryotic cells. , 1992 .

[43]  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.

[44]  R De Wachter,et al.  DCSE, an interactive tool for sequence alignment and secondary structure research. , 1993, Computer applications in the biosciences : CABIOS.

[45]  S. P. Gibbs,et al.  EVIDENCE THAT THE NUCLEOMORPHS OF CHLORARACHNION REPTANS (CHLORARACHNIOPHYCEAE) ARE VESTIGIAL NUCLEI: MORPHOLOGY, DIVISION AND DNA‐DAPI FLUORESCENCE 1 , 1989 .

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

[47]  Hervé Philippe,et al.  Early–branching or fast–evolving eukaryotes? An answer based on slowly evolving positions , 2000, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[48]  T. Cavalier-smith Membrane heredity, symbiogenesis, and the multiple origins of algae , 1995 .

[49]  M. Allard,et al.  The production of single-stranded DNA suitable for sequencing using the polymerase chain reaction. , 1991, BioTechniques.

[50]  Y Van de Peer,et al.  Substitution rate calibration of small subunit ribosomal RNA identifies chlorarachniophyte endosymbionts as remnants of green algae. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[51]  T. Cavalier-smith,et al.  Single gene circles in dinoflagellate chloroplast genomes , 1999, Nature.

[52]  D. Hibberd,et al.  A NEW ALGAL CLASS — THE EUSTIGMATOPHYCEAE , 1971 .

[53]  R. Andersen,et al.  Phylogeny of the Eustigmatophyceae Based upon 18S rDNA, with Emphasis on Nannochloropsis. , 1998, Protist.

[54]  K. Strimmer,et al.  Quartet Puzzling: A Quartet Maximum-Likelihood Method for Reconstructing Tree Topologies , 1996 .

[55]  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.

[56]  M. Sogin,et al.  A NEW PHYLOGENY FOR CHROMOPHYTE ALGAE USING 16S‐LIKE RRNA SEQUENCES FROM MALLOMONAS PAPILLOSA (SYNUROPHYCEAE) AND TRIBONEMA AEQUALE (XANTHOPHYCEAE) 1 , 1991 .

[57]  M. Sogin,et al.  Molecular phylogenetic analysis of actin genic regions from Achlya bisexualis (Oomycota) and Costaria costata (Chromophyta). , 1991, Journal of molecular evolution.

[58]  Detlef D. Leipe,et al.  The stramenopiles from a molecular perspective 16S-like rRNA sequences from Labyrinthuloides minuta and Cafeteria roenbergensis , 1994 .

[59]  N. Saitou,et al.  The neighbor-joining method: a new method for reconstructing phylogenetic trees. , 1987, Molecular biology and evolution.

[60]  R De Wachter,et al.  RnaViz, a program for the visualisation of RNA secondary structure. , 1997, Nucleic acids research.

[61]  J. Palmer,et al.  The Origin and Evolution of Plastids and Their Genomes , 1998 .

[62]  T. Cavalier-smith,et al.  Thraustochytrids are Chromists, not Fungi: 18s rRNA Signatures of Heterokonta , 1994 .

[63]  R. Andersen,et al.  Phylogenetic relationships of the Raphidophyceae and Xanthophyceae as inferred from nucleotide sequences of the 18S ribosomal RNA gene. , 1997, American journal of botany.

[64]  H Philippe,et al.  Phylogeny of eukaryotes based on ribosomal RNA: long-branch attraction and models of sequence evolution. , 2000, Molecular biology and evolution.

[65]  G. McFadden,et al.  The miniaturized nuclear genome of eukaryotic endosymbiont contains genes that overlap, genes that are cotranscribed, and the smallest known spliceosomal introns. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[66]  R. Andersen,et al.  PHYLOGENETIC AFFINITIES OF THE SARCINOCHRYSIDALES AND CHRYSOMERIDALES (HETEROKONTA) BASED ON ANALYSES OF MOLECULAR AND COMBINED DATA 1 , 1997 .

[67]  T. Cavalier-smith,et al.  18S rRNA sequence of Heterosigma carterae (Raphidophyceae), and the phylogeny of heterokont algae (Ochrophyta) , 1996 .

[68]  T. Cavalier-smith,et al.  Chimeric conundra: are nucleomorphs and chromists monophyletic or polyphyletic? , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[69]  R. Andersen,et al.  A MOLECULAR PHYLOGENY OF THE HETEROKONT ALGAE BASED ON ANALYSES OF CHLOROPLAST‐ENCODED rbcL SEQUENCE DATA 1 , 1997 .

[70]  D. Spencer,et al.  Cryptomonad algae are evolutionary chimaeras of two phylogenetically distinct unicellular eukaryotes , 1991, Nature.

[71]  D. Hibberd,et al.  Eustigmatophyceae—a New Algal Class with Unique Organization of the Motile Cell , 1970, Nature.

[72]  S. Chapelle,et al.  Structure of the large ribosomal subunit RNA of Phytophthora megasperma, and phylogeny of the oomycetes , 1994, FEBS letters.

[73]  Y. van de Peer,et al.  Construction of evolutionary distance trees with TREECON for Windows: accounting for variation in nucleotide substitution rate among sites. , 1997, Computer applications in the biosciences : CABIOS.

[74]  Detlef D. Leipe,et al.  16S-like rDNA sequences from Developayella elegans, Labyrinthuloides haliotidis, and Proteromonas lacertae confirm that the stramenopiles are a primarily heterotrophic group , 1996 .