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The Complete Chloroplast DNA Sequence of the Green Alga Nephroselmis Olivacea: Insights Into the Architecture of Ancestral Chloroplast Genomes

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The Complete Chloroplast DNA Sequence of the Green Alga Nephroselmis Olivacea: Insights Into the Architecture of Ancestral Chloroplast Genomes Proc. Natl. Acad. Sci. USA Vol. 96, pp. 10248–10253, August 1999 Evolution The complete chloroplast DNA sequence of the green alga Nephroselmis olivacea: Insights into the architecture of ancestral chloroplast genomes MONIQUE TURMEL*, CHRISTIAN OTIS, AND CLAUDE LEMIEUX Canadian Institute for Advanced Research, Program in Evolutionary Biology and De´partementde Biochimie, Universite´Laval, Que´bec, QC, G1K 7P4, Canada Edited by Robert Haselkorn, University of Chicago, Chicago, IL, and approved June 28, 1999 (received for review April 13, 1999) ABSTRACT Green plants seem to form two sister lin- primary chloroplasts of glaucocystophytes evolved before the eages: Chlorophyta, comprising the green algal classes Pra- divergence of the red and green algae and that the secondary sinophyceae, Ulvophyceae, Trebouxiophyceae, and Chloro- chloroplasts of heterokonts were derived from a red alga (14). phyceae, and Streptophyta, comprising the Charophyceae and Given the important differences in structure, gene content and land plants. We have determined the complete chloroplast gene organization between the cpDNAs examined thus far, it DNA (cpDNA) sequence (200,799 bp) of Nephroselmis olivacea, is difficult to predict the cpDNA architecture of the common a member of the class (Prasinophyceae) thought to include ancestor of glaucocystophytes, red algae, and green algae. descendants of the earliest-diverging green algae. The 127 With 251 genes, Porphyra cpDNA is the most gene-rich genes identified in this genome represent the largest gene cpDNA; in contrast, Euglena, Chlorella, and land plant cp- repertoire among the green algal and land plant cpDNAs DNAs contain many fewer genes (97–110). Gene loss has been completely sequenced to date. Of the Nephroselmis genes, 2 an ongoing process in all algal lineages, with independent (ycf81 and ftsI, a gene involved in peptidoglycan synthesis) parallel losses occurring in multiple lineages (14). have not been identified in any previously investigated cpDNA; Considering that the unicellular progenitors of land plants 5 genes [ftsW, rnE, ycf62, rnpB, and trnS(cga)] have been found lie within the green algae, deciphering the evolutionary history only in cpDNAs of nongreen algae; and 10 others (ndh genes) of cpDNA within this algal group is of particular interest. have been described only in land plant cpDNAs. Nephroselmis Phycologists generally recognize five green algal classes: Cha- and land plant cpDNAs share the same quadripartite struc- rophyceae, which include the closest relatives of land plants, ture—which is characterized by the presence of a large Chlorophyceae, Trebouxiophyceae, Ulvophyceae, and a non- rRNA-encoding inverted repeat and two unequal single-copy monophyletic group known as Prasinophyceae (13, 15, 16). All regions—and very similar sets of genes in corresponding extant green algae are thought to belong to two major evolu- genomic regions. Given that our phylogenetic analyses place Nephroselmis within the Chlorophyta, these structural char- tionary lineages: Streptophyta, containing the charophytes, acteristics were most likely present in the cpDNA of the land plants, and possibly some prasinophytes, and Chloro- common ancestor of chlorophytes and streptophytes. Com- phyta, containing the rest of the algae. Prasinophytes are parative analyses of chloroplast genomes indicate that the considered to represent the earliest offshoots of the chloro- typical quadripartite architecture and gene-partitioning pat- phyte lineage. tern of land plant cpDNAs are ancient features that may have The cpDNA sequence of the trebouxiophyte Chlorella (11) been derived from the genome of the cyanobacterial progen- and the fragmentary cpDNA data available from a few mem- itor of chloroplasts. Our phylogenetic data also offer insight bers of the Charophyceae, Ulvophyceae, and Chlorophyceae into the chlorophyte ancestor of euglenophyte chloroplasts. indicate that green algal cpDNAs evolve in a much less conservative fashion compared with their land plant counter- Complete chloroplast DNA (cpDNA) sequences have been parts (17). These data preclude any prediction regarding the determined for five land plants (Marchantia polymorpha, ref. 1; cpDNA architecture of the most ancestral green algae. Pinus thunbergii, ref. 2; Nicotiana tabacum, ref. 3; Oryza sativa, Whether one of the structural landmarks of the ancestral green ref. 4; and Zea mays, ref. 5) and for six algae from different algal genome was an rRNA operon-encoding inverted repeat lineages (the glaucocystophyte Cyanophora paradoxa, ref. 6; (IR) homologous to that dominating the architecture of most the red alga Porphyra purpurea, ref. 7; the heterokont Odontella land plant cpDNAs is unknown (12, 17). sinensis, ref. 8; the cryptophyte Guillardia theta, ref. 9; the Here, we report the complete cpDNA sequence of the euglenophyte Euglena gracilis, ref. 10; and the green alga prasinophyte Nephroselmis olivacea. This green algal cpDNA Chlorella vulgaris, ref. 11). These sequence data support the and its land plant homologs share the same quadripartite view that all chloroplasts were derived from a single primary structure—which is defined by the presence of two copies of an endosymbiotic event involving the capture of a cyanobacte- IR sequence separated by unequal single-copy regions—and rium (12, 13). The chloroplasts of glaucocystophytes, red algae, very similar sets of genes in corresponding genomic regions. As and green algae are thought to be direct products of this Nephroselmis is a member of the Chlorophyta, our results primary endosymbiotic event, and secondary endosymbioses provide insight into the cpDNA organization of the ancestral involving the capture of photosynthetic algae have been pos- green algae that appeared before the divergence of the Chlo- tulated for the origin of heterokont, cryptophyte, and eugleno- rophyta and Streptophyta. Our results also suggest that the IR phyte chloroplasts (12, 13). A phylogenetic analysis of 45 and pattern of gene partitioning in the ancestral green algal protein-coding genes common to all cpDNAs sequenced thus far, except those of Chlorella and Guillardia, indicates that the This paper was submitted directly (Track II) to the Proceedings office. Abbreviations: cpDNA, chloroplast DNA; IR, inverted repeat; LSC, The publication costs of this article were defrayed in part by page charge large single-copy; SSC, small single-copy. Data deposition: The sequence reported in this paper has been payment. This article must therefore be hereby marked ‘‘advertisement’’ in deposited in the GenBank database (accession no. AF137379). accordance with 18 U.S.C. §1734 solely to indicate this fact. *To whom reprint requests should be addressed. E-mail: monique. PNAS is available online at www.pnas.org. [email protected]. 10248 Downloaded by guest on September 27, 2021 Evolution: Turmel et al. Proc. Natl. Acad. Sci. USA 96 (1999) 10249 genome trace their origin to the chloroplasts of the common assembled with AUTOASSEMBLER 1.4.0 (Applied Biosystems) ancestor of glaucocystophytes, red algae, and green algae. and analyzed with the Genetics Computer Group software (Version 9.1, Madison, WI). Statistical analyses of codon usage MATERIALS AND METHODS and base composition at first and third codon positions were performed as described (19). As the nuclear and organelle DNAs of N. olivacea (NIES-484) Multiple protein alignments were carried out with CLUST- could not be resolved in CsCl-bisbenzimide gradients, a library ALW 1.74 (20). Protein alignments were concatenated; ambig- of total cellular DNA was prepared by ligating partially uously aligned regions were deleted; and phylogenetic analyses digested and partially filled-in MboI fragments to Lambda- were performed with PROTML in MOLPHY 2.3B3 (J. Adachi and GEM-11 (Promega; ref. 18). Clones carrying cpDNA inserts M. Hasegawa, Institute of Statistical Mathematics, Tokyo) and were first identified by hybridization with Chlamydomonas the JTT-F model of amino acid replacement. The bootstrap cpDNA fragments specific to various genes. These clones method of resampling of the estimated log-likelihood was used served as starting points for genome walks undertaken to to assess the statistical significance of tree topologies. assemble a collection of clones encompassing Nephroselmis cpDNA—by using, as probes, PCR-amplified fragments com- RESULTS AND DISCUSSION plementary to the termini of selected inserts or long PCR- amplified fragments covering gaps between contigs. Numerous Structure and Gene Content of Nephroselmis cpDNA. The clones from each round of hybridization were selected for Nephroselmis cpDNA sequence assembles as a circle of 200,799 DNA isolation (18). bp, with an overall A ϩ T content of 57.9% (Fig. 1). Two All sequences were determined with the PRISM dye ter- identical copies of a large sequence (46,137 bp) containing the minator cycle sequencing kit (Applied Biosystems) on the ABI rRNA operon are present in inverted orientation and are model 373 DNA sequencer (Applied Biosystems). Both ends separated from one another by LSC (92,126 bp) and SSC of each insert were sequenced with T7 and SP6 primers, (16,399 bp) regions. Such a quadripartite structure is found in whereas internal regions were sequenced by the primer- the completely sequenced cpDNAs of Cyanophora, Odontella, walking method with specific 22-mer oligonucleotides. Guillardia, and land plants, as well as in numerous algal and Genomic regions not represented in the clones analyzed were land plant cpDNAs that
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