DISCONTINUOUS MITOCHONDRIAL AND CHLOROPLAST LARGE SUBUNIT RIBOSOMAL RNAs AMONG GREEN ALGAE: PHYLOGENETIC IMPLICATIONS1 (original) (raw)
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Journal of Phycology, 1998
The three green algal mitochondrial genomes completely sequenced to date-those of Chlamydomonas reinhardtii Dangeard, Chlamydomonas eugametos Gerloff, and Prototheca wickerhamii Soneda & Tubaki-revealed very different mitochondrial genome organizations and sequence affiliations. The Chlamydomonas genomes resemble the ciliate/fungal/animal counterparts, and the Prototheca genome resembles land plant homologues. This review points out that all the green algal mitochondrial genomes examined to date resemble either the Chlamydomonas or the Prototheca mitochondrial genome; the Chlamydomonas-like mitochondrial genomes are small and have a reduced gene content (no ribosomal protein or 5S rRNA genes and only a few protein-coding and tRNA genes) and fragmented and scrambled rRNA coding regions, whereas the Prototheca-like mitochondrial genomes are larger and have a larger set of protein-coding genes (including ribosomal protein genes), more tRNA genes, and 5S rRNA and conventional continuous smallsubunit (SSU) and large-subunit (LSU) rRNA coding regions. It appears, therefore, that the differences previously observed between the mitochondrial genomes of C. reinhardtii and P. wickerhamii extend to the two green algal mitochondrial lineages to which they belong and are significant enough to raise questions about the causes and mechanisms responsible for such contrasting evolutionary strategies among green algae. This review suggests an integrative approach in explaining the occurrence of distinct evolutionary strategies and apparent phylogenetic affiliations among the known green algal mitochondrial lineages. The observed differences could be the result of distinct genetic potentials differentiated during the previous evolutionary history of the flagellate ancestors and/or of subsequent changes in habitat and life history of the more advanced green algal lineages.
Evolution of fragmented mitochondrial ribosomal RNA genes inChlamydomonas
Journal of Molecular Evolution, 1996
The fragmented mitochondrial ribosomal RNAs (rRNAs) of the green algae Chlamydomonas eugametos and Chlamydomonas reinhardtii are discontinuously encoded in subgenic modules that are scrambled in order and interspersed with protein coding and tRNA genes. The mitochondrial rRNA genes of these two algae differ, however, in both the distribution and organization of rRNA coding information within their respective genomes. The objectives of this study were (1) to examine the phylogenetic relationships between the mitochondrial rRNA gene sequences of C. eugametos and C. reinhardtii and those of the conventional mitochondrial rRNA genes of the green alga, Prototheca wickerhamii, and land plants and (2) to attempt to deduce the evolutionary pathways that gave rise to the unusual mitochondrial rRNA gene structures in the genus Chlamydomonas. Although phylogenetic analysis revealed an affiliation between the mitochondrial rRNA gene sequences of the two Chlamydomonas taxa to the exclusion of all other mitochondrial rRNA gene sequences tested, no specific affiliation was noted between the Chlamydomonas sequences and P. wickerhamii or land plants. Calculations of the minimal number of transpositions required to convert hypothetical ancestral rRNA gene organizations to the arrangements observed for C. eugametos and C. reinhardtii mitochondrial rRNA genes, as well as a limited survey of the size of mitochondrial rRNAs in other members of the genus, lead us to propose that the last common ancestor of Chlamydomonas algae contained fragmented mitochondrial rRNA genes that were nearly co-linear with conventional rRNA genes.
Polyphyly of Tetrasporalean Green Algae Inferred from Nuclear Small-Subunit Ribosomal Dna
Journal of Phycology, 1998
Ultrastructural studies of tetrasporalean green algae have suggested the order is polyphyletic. These features, including the absolute orientation of the flagellar apparatus and the bi-versus quadriflagellated motile cell morphology, suggest that Chaetopeltis as well as a number of others, may be ancestral to a group that includes Tetraspora. In this study, we examine the phylogenetic relationships of selected tetrasporalean taxa based on analysis of 18S ribosomal RNA gene sequences. Results show that the tetrasporalean taxa are polyphyletic. Biflagellated genera group with biflagellated volvocalean taxa, whereas the quadriflagellated species compose a distinct monophyletic clade not closely related to the biflagellated taxa. In addition, tetrasporalean taxa group with other chlorophycean algal species with similar flagellar apparatus absolute orientation, but the quadriflagellated Tetrasporales do not appear to be ancestral to the entire Chlorophyceae. These results are concordant with previous conclusions drawn from ultrastructural data and further confirm the utility of (small-subunit) ribosomal RNA gene sequences to discern green algal evolutionary relationships.
Protist, 1998
The prasinophytes comprise a morphologically heterogeneous assembly of mostly marine flagellates and coccoid taxa, which represent an important component of the nano-and picoplankton, and have previously figured prominently in discussions about the origin and phylogeny of the green plants. To evaluate their putative basal position in the Viridiplantae and to resolve the phylogenetic relationships among the prasinophyte taxa, we determined complete nuclear-encoded SSU rRNA sequences from 13 prasinophyte taxa representing the genera Cymbomonas, Halosphaera, Mamiella, Mantoniella, Micromonas, Pterosperma, Pycnococcus, and Pyramimonas. Phylogenetic analyses of SSU rRNA sequences using distance, parsimony and likelihood methods revealed four independent prasinophyte lineages (clades) which constitute the earliest divergences among the Chlorophyta. In order of their divergence these clades are represented by the genera Cymbomonas, Halosphaera, Pterosperma, Pyramimonas (clade I), Mamiella, Mantoniella, Micromonas (clade II), Pseudoscourfie/dia (strain CCMP 717), Nephroselmis (clade III), and Tetraselmis, Scherffelia (clade IV). The coccoid Pycnococcus provasolii diverged after clade II, but before clade III. Since no other coccoid prasinophyte taxa were analyzed in this study, the phylogenetic status of this taxon is presently unresolved. Our analyses provide further evidence for the basal phylogenetic position of the scaly green flagellates among the Chlorophyta and raise important questions concerning the class-level classification of the Chlorophyta.
Genome …, 2000
Two distinct mitochondrial genome types have been described among the green algal lineages investigated to date: a reduced-derived, Chlamydomonas-like type and an ancestral, Prototheca-like type. To determine if this unexpected dichotomy is real or is due to insufficient or biased sampling and to define trends in the evolution of the green algal mitochondrial genome, we sequenced and analyzed the mitochondrial DNA (mtDNA) of Scenedesmus obliquus. This genome is 42,919 bp in size and encodes 42 conserved genes (i.e., large and small subunit rRNA genes, 27 tRNA and 13 respiratory protein-coding genes), four additional free-standing open reading frames with no known homologs, and an intronic reading frame with endonuclease/maturase similarity. No 5S rRNA or ribosomal protein-coding genes have been identified in Scenedesmus mtDNA. The standard protein-coding genes feature a deviant genetic code characterized by the use of UAG (normally a stop codon) to specify leucine, and the unprecedented use of UCA (normally a serine codon) as a signal for termination of translation. The mitochondrial genome of Scenedesmus combines features of both green algal mitochondrial genome types: the presence of a more complex set of protein-coding and tRNA genes is shared with the ancestral type, whereas the lack of 5S rRNA and ribosomal protein-coding genes as well as the presence of fragmented and scrambled rRNA genes are shared with the reduced-derived type of mitochondrial genome organization. Furthermore, the gene content and the fragmentation pattern of the rRNA genes suggest that this genome represents an intermediate stage in the evolutionary process of mitochondrial genome streamlining in green algae.
Journal of Molecular Biology, 1996
Except in the case of land plants, mitochondrial ribosomes apparently lack Université de Montréal a 5 S rRNA species, even though this small RNA is a component of all prokaryotic, chloroplast and eukaryotic cytosol ribosomes. In plants, the Montréal, Québec H3C 3J7 Canada mitochondrial 5 S rRNA is encoded by mtDNA and differs in sequence from the 5 S rRNA specified by plant nuclear and chloroplast genomes. A distinctive 5 S rRNA component has not been found in the mitochondrial University of California at ribosomes of non-plant eukaryotes and, with the notable exception of the Santa Cruz, Santa Cruz chlorophycean alga, Prototheca wickerhamii, a 5 S rRNA gene has not been CA 95064, USA identified in those non-plant mtDNAs characterized to date. Here, we report the presence of a 5 S rRNA gene in the mtDNA of the heterotrophic 3 Department of Biochemistry flagellate Reclinomonas americana. This unicellular eukaryote is a member Dalhousie University, Halifax of the jakobid flagellates, an early-diverging group of protists that share Nova Scotia B3H 4H7
Molecular Biology and Evolution, 1998
Current data on green algal mitochondrial genomes suggest an unexpected dichotomy within the group with respect to genome structure, organization, and sequence affiliations. The present study suggests that there is a correlation between this dichotomy on one hand and the differences in the abundance, base composition, and distribution of short repetitive sequences we observed among green algal mitochondrial genomes on the other. It is conceivable that the accumulation of GC-rich short repeated sequences in the Chlamydomonas-like but not Prototheca-like mitochondrial genomes might have triggered evolutionary events responsible for the distinct series of evolutionary changes undergone by the two green algal mitochondrial lineages. The similarity in base composition, nucleotide sequence, abundance, and mode of organization we observed between the short repetitive sequences present in Chlamydomonas-like mitochondrial genomes on one hand and fungal and vertebrate homologs on the other might extend to some of the roles that the short repetitive sequences have been shown to have in the latter. Potential involvements we propose for the short repetitive sequences in the evolution of Chlamydomonas-like mitochondrial genomes include fragmentation and scrambling of the ribosomal-RNA-coding regions, extensive gene rearrangements, coding-region deletions, surrogate origins of replication, and chromosomal linearization.
Complex Patterns of Plastid 16S rRNA Gene Evolution in Nonphotosynthetic Green Algae
Journal of Molecular Evolution, 2001
This study provides a phylogenetic/ comparative approach to deciphering the processes underlying the evolution of plastid rRNA genes in genomes under relaxed functional constraints. Nonphotosynthetic green algal taxa that belong to two distinct classes, Chlorophyceae (Polytoma) and Trebouxiophyceae (Prototheca), were investigated. Similar to the situation described previously for plastid 16S rRNA genes in nonphotosynthetic land plants, nucleotide substitution levels, extent of structural variations, and percentage AT values are increased in nonphotosynthetic green algae compared to their closest photosynthetic relatives. However, the mutational processes appear to be different in many respects. First, with the increase in AT content, more transversions are noted in Polytoma and holoparasite angiosperms, while more transitions characterize the evolution of the 16S rDNA sequences in Prototheca. Second, although structural variations do accumulate in both Polytoma and Prototheca (as well as holoparasitic plastid 16S rRNAs), insertions as large as 1.6 kb characterize the plastid 16S rRNA genes in the former, whereas significantly smaller indels (not exceeding 24 bp) seem to be more prevalent in the latter group. The differences in evolutionary rates and patterns within and between lineages might be due to mutations in replication/repair-related genes; slipped-strand mispairing is likely the mechanism responsible for the expansion of insertions in Polytoma plastid 16S rRNA genes.
Molecular Biology and Evolution, 1997
Using the large subunit of RuBisCo (&CL) sequences from cyanobacteria, proteobacteria, and diverse groups of algae and green plants, we evaluated the plastid relationship between haptophytes and heterokont algae. The &CL sequences were determined from three taxa of heterokont algae (Bumilleriopsis jiliformis, Pelagomonas calceolata, and Pseudopedinella elastica) and added to 25 published sequences to obtain a data set comprising 1,434 unambiguously aligned sites (-98% of the total rbcL gene). Higher levels of mutational saturation in third codon positions were observed by plotting the pairwise substitutions with and without corrections for multiple substitutions at the same site for first and second codon positions only and for third positions only. In accordance with this finding phylogeny reconstructions were completed by omitting third codon positions, thus using 956 bp in weightedparsimony and maximum-likelihood analyses. The midpoint-rooted phylogenies showed two major clusters, one containing cyanobacteria, glaucocystophytes, a phototrophic euglenoid, chlorophytes, and embryophytes (the green lineage), the other containing proteobacteria, haptophytes, red algae, a cryptophyte, and heterokont algae (the nongreen lineage). In the nongreen lineage, the haptophytes formed a sister group to the clade containing heterokont algae, red algae, and the cryptophyte GuiZZardia theta. This branching pattern was well supported in terms of bootstrap values in weighted-parsimony and maximum-likelihood analyses (100% and 92%, respectively). However, the phylogenetic relationship among red algae, heterokonts, and a cryptophyte taxon was not especially well resolved. A four-cluster analysis was performed to further explore the statistical significance of the relationship between proteobacteria, red algae (including and excluding GuiZZardia theta), haptophytes, and heterokont algae. This test strongly favored the hypothesis that the heterokonts and red algae are more closely related to each other than either is to proteobacteria or haptophytes. Hence, this molecular study based on a plastid-encoded gene provides additional evidence for a distant relationship between haptophytes and the heterokont algae. It suggests an evolutionary scenario in which the ancestor of the haptophyte lineage engulfed a phototrophic eukaryote and, more recently, the heterokont lineage became phototrophic by engulfing a red alga.