The complete chloroplast DNA sequence of the green alga Oltmannsiellopsis viridis reveals a distinctive quadripartite architecture in the chloroplast genome of early diverging ulvophytes
© Pombert et al; licensee BioMed Central Ltd. 2006
Received: 17 November 2005
Accepted: 03 February 2006
Published: 03 February 2006
The phylum Chlorophyta contains the majority of the green algae and is divided into four classes. The basal position of the Prasinophyceae has been well documented, but the divergence order of the Ulvophyceae, Trebouxiophyceae and Chlorophyceae is currently debated. The four complete chloroplast DNA (cpDNA) sequences presently available for representatives of these classes have revealed extensive variability in overall structure, gene content, intron composition and gene order. The chloroplast genome of Pseudendoclonium (Ulvophyceae), in particular, is characterized by an atypical quadripartite architecture that deviates from the ancestral type by a large inverted repeat (IR) featuring an inverted rRNA operon and a small single-copy (SSC) region containing 14 genes normally found in the large single-copy (LSC) region. To gain insights into the nature of the events that led to the reorganization of the chloroplast genome in the Ulvophyceae, we have determined the complete cpDNA sequence of Oltmannsiellopsis viridis, a representative of a distinct, early diverging lineage.
The 151,933 bp IR-containing genome of Oltmannsiellopsis differs considerably from Pseudendoclonium and other chlorophyte cpDNAs in intron content and gene order, but shares close similarities with its ulvophyte homologue at the levels of quadripartite architecture, gene content and gene density. Oltmannsiellopsis cpDNA encodes 105 genes, contains five group I introns, and features many short dispersed repeats. As in Pseudendoclonium cpDNA, the rRNA genes in the IR are transcribed toward the single copy region featuring the genes typically found in the ancestral LSC region, and the opposite single copy region harbours genes characteristic of both the ancestral SSC and LSC regions. The 52 genes that were transferred from the ancestral LSC to SSC region include 12 of those observed in Pseudendoclonium cpDNA. Surprisingly, the overall gene organization of Oltmannsiellopsis cpDNA more closely resembles that of Chlorella (Trebouxiophyceae) cpDNA.
The chloroplast genome of the last common ancestor of Oltmannsiellopsis and Pseudendoclonium contained a minimum of 108 genes, carried only a few group I introns, and featured a distinctive quadripartite architecture. Numerous changes were experienced by the chloroplast genome in the lineages leading to Oltmannsiellopsis and Pseudendoclonium. Our comparative analyses of chlorophyte cpDNAs support the notion that the Ulvophyceae is sister to the Chlorophyceae.
The green algae are divided into the phyla Streptophyta and Chlorophyta. The Streptophyta (sensu Bremer ) encompasses the algae from the class Charophyceae and all land plants, whereas the Chlorophyta (sensu Sluiman ) contains algae from the classes Prasinophyceae, Ulvophyceae, Trebouxiophyceae and Chlorophyceae . The basal position of the Prasinophyceae in the Chlorophyta is generally well established, but the branching order of the Ulvophyceae, Trebouxiophyceae and Chlorophyceae (UTC) remains a matter of debate [4–6]. It has been proposed that a third lineage at the base of the Streptophyta and Chlorophyta is represented by Mesostigma viride [7–9], an alga traditionally classified within the prasinophytes. This green plant lineage, however, is debated, as some studies suggest that Mesostigma is an early offshoot of the phylum Streptophyta [10–12].
Investigations of chloroplast DNA (cpDNA) from green algae representing each of the five recognized classes have revealed that the genomes of the charophyte Chaetosphaeridium globosum  and the prasinophytes Mesostigma  and Nephroselmis olivacea  are highly similar to those of land plants. Like most land plants cpDNAs, these green algal genomes are partitioned into a quadripartite architecture by two copies of a large inverted repeat (IR) separating small (SSC) and large (LSC) single copy regions. Most notably, the great majority of the genes occupying a given single copy region in prasinophyte genomes map to the same single copy region in Chaetosphaeridium and land plant cpDNAs. The increased structural stability of the chloroplast genome conferred by the IR sequence has been hypothesized to limit gene exchanges between the SSC and LSC regions . The IR region readily expands or contracts and thus can easily gain or lose genes from the neighbouring single copy regions through a process known as the ebb and flow . Despite its variable gene content, the IR always features the ribosomal RNA (rRNA) operon (rrs-I(gau)-A(ugc)-rrl-rrf) and this operon is always transcribed toward the SSC region. In addition to their characteristic pattern of gene partitioning, prasinophyte and streptophyte chloroplast genomes share a number of features that were most probably inherited from the progenitor of all green plant cpDNAs. First, they have retained several gene clusters that date back to the cyanobacterial ancestor of all chloroplasts. Second, their genes are densely packed and their intergenic regions virtually lack short dispersed repeats (SDRs). Finally, with 128 to 137 genes, their gene repertoire is one of the largest among green plant cpDNAs.
In contrast, the chloroplast genome has been substantially reorganized in the UTC. The quadripartite architecture has been lost from the genome of the trebouxiophyte Chlorella vulgaris  following the disappearance of one copy of the IR sequence. Although the quadripartite architecture has been retained in the genome of the ulvophyte Pseudendoclonium akinetum , the IR sequence is atypical in featuring a rRNA operon transcribed towards the LSC region . In addition, the pattern of gene partitioning within the SSC/LSC regions of Pseudendoclonium cpDNA deviates significantly from those found in its prasinophyte and land plant counterparts; the small single copy region of this ulvophyte genome includes 14 genes that are usually located within the LSC region. In the chlorophycean alga Chlamydomonas reinhardtii , the two single copy regions are similar in size and the genes are so thoroughly scrambled that no distinction is possible between the SSC and LSC regions. The Chlorella, Pseudendoclonium and Chlamydomonas chloroplast genomes have lost many of the ancestral gene clusters that are shared between Mesostigma and Nephroselmis cpDNAs, feature a reduced gene content (from 94 genes in Chlamydomonas to 112 genes in Chlorella) compared to prasinophyte and streptophyte genomes, and contain SDRs in their intergenic regions. The low density of coding sequences in these genomes is explained not only by the smaller number of genes but also by the expansion of intergenic regions. Moreover, unlike Mesostigma and Nephroselmis cpDNAs, the chloroplast genomes of the three UTC algae have acquired group I introns (from three in Chlorella to 27 in Pseudendoclonium) and group II introns (two in Chlamydomonas).
To gain insights into the nature of the events that led to the reorganization of the chloroplast genome in the Ulvophyceae, we have determined the complete cpDNA sequence of Oltmannsiellopsis viridis. This marine unicellular green alga exhibits a counterclockwise arrangement of basal bodies [19, 20] and a single cup-shaped chloroplast . Previously classified in the Chlorophyceae [19, 21], Oltmannsiellopsis is currently considered to be the type species of the order Oltmannsiellopsidales (Ulvophyceae) . The Oltmannsiellopsidales have been shown to branch at the base of the Ulvophyceae  and have been used as outgroup for phylogenetic analyses of the Ulvophyceae [23–25]. Considering that Pseudendoclonium represents a distinct, early diverging lineage of the Ulvophyceae (Ulotrichales, see supplementary Figure S1 in ), identification of the set of features common to Oltmannsiellopsis and Pseudendoclonium cpDNAs should throw light into the chloroplast genome architecture of the earliest diverging ulvophytes and, accordingly, into the cpDNA changes that occurred in the separate lineages leading to Oltmannsiellopsis and Pseudendoclonium. We found that the IR-containing genome of Oltmannsiellopsis differs considerably from its Pseudendoclonium and other chlorophyte counterparts in intron content and gene order, but shares closer similarities with Pseudendoclonium cpDNA in terms of quadripartite architecture, gene content and gene density. In the context of the debate concerning the branching order of the UTC lineages, the predicted architecture of the chloroplast genome of the earliest members of the Ulvophyceae strengthens the notion that this lineage is sister to the Chlorophyceae [5, 6].
Results and discussion
General features of Oltmannsiellopsis and other chlorophyte cpDNAs
Coding sequences (%)c
Gene and intron contents
Differences between the gene repertoires of Oltmannsiellopsis and other UTC algal cpDNAs
Compared sizes of expanded genes in Oltmannsiellopsis and other UTC algal cpDNAs
Group I introns in Oltmannsiellopsis cpDNA
Group I introns at identical gene locations in Oltmannsiellopsis cpDNA, other green algal cpDNAs and land plant cpDNAs
Green planta/Intron numberb
Pseudendoclonium akinetum i5 (U)
Chlamydomonas reinhardtii i3 (C)
Chlamydomonas geitleri (C)
Dunaliella parva i2 (C)
Haematococcus lacustris i3 (C)
Chlamydomonas callosa i3 (C)
Chlamydomonas komma i2 (C)
Chlamydomonas mexicana i1 (C)
Chlamydomonas frankii i2 (C)
Chlamydomonas pallidostigmatica i2 (C)
Neochloris aquatica i2 (C)
Chlorosarcina brevispinosa i2 (C)
Pedinomonas tuberculata i1 (?)
Monomastix species M722 i1 (P)
Monomastix species OKE-1 i1 (P)
Pterosperma cristatum (P)
Chlamydomonas monadina i3 (C)
Chlamydomonas humicola (C)
Dunaliella parva i4 (C)
Chlamydomonas zebra (C)
Chlamydomonas starrii (C)
Chlamydomonas frankii i4 (C)
Neochloris aquatica i3 (C)
Ankistrodesmus stipitatus i2 (C)
Stigeoclonium helveticum i4 (C)
Trebouxia aggregata i2 (T)
Trichosarcina mucosa i1 (U)
Pedinomonas tuberculata i3 (?)
Monomastix species OKE-1 i3 (P)
Chlamydomonas agloeformis (C)
Chlamydomonas callosa i4 (C)
Chlamydomonas iyengarii (C)
Chlamydomonas mexicana i2 (C)
Chlamydomonas nivalis (C)
Chlamydomonas peterfii (C)
Chlamydomonas reinhardtii (C)
Carteria lunzensis (C)
Carteria olivieri (C)
Haematococcus lacustris i4 (C)
Pediastrum biradiatum (C)
Neochloris aquatica i4 (C)
Scenedesmus obliquus (C)
Pseudendoclonium akinetum (U)
Trichosarcina mucosa i2 (U)
Chlorella vulgaris (T)
Monomastix species M722 i3 (P)
Monomastix species OKE-1 i4 (P)
Scherffelia dubia (P)
Anthoceros punctatus (E)
Anthoceros formosae (E)
Genome structure and gene partitioning
The pattern of gene partitioning within the single copy regions of Oltmannsiellopsis cpDNA differs substantially from the ancestral partitioning pattern observed for Mesostigma, Nephroselmis and streptophyte cpDNAs (Figure 1). The great majority of the 30 genes found in the SC1 region of Oltmannsiellopsis are typically found in the ancestral LSC region, whereas the SC2 region contains 52 genes characteristic of the ancestral LSC region in addition to ten genes characteristic of the ancestral SSC region. Interestingly, SC2 includes 12 of the 14 LSC genes that have been transferred to the SSC region in Pseudendoclonium cpDNA. The two exceptional Pseudendoclonium genes that have no homologues in Oltmannsiellopsis SC2 are trnH(gug) and trnL(caa); the trnH(gug) gene resides in the SC1 region of Oltmannsiellopsis, whereas trnL(caa) has been lost from Oltmannsiellopsis cpDNA. Considering the gene contents of the Oltmannsiellopsis single copy regions, it appears inappropriate to label these regions according to their sizes. Although SC1 is smaller than SC2, it likely corresponds to the ancestral LSC region, and SC2 is apparently derived from the ancestral SSC region.
The IR sequence in Oltmannsiellopsis cpDNA is about 12 kb larger than that in Pseudendoclonium cpDNA and contains five genes in addition to those found in the rRNA operon (Figure 1). At 18,510 bp, the IR sequence of Oltmannsiellopsis is similar in size to that of Chlamydomonas (Table 1). Both IR junctions in Oltmannsiellopsis cpDNA encompass genes (cemA and ftsH) of which the coding sequences expand into the single copy regions. As in the Pseudendoclonium IR, the Oltmannsiellopsis rRNA genes are transcribed towards the single copy region carrying the genes that map to the LSC in prasinophyte and streptophyte cpDNAs. In contrast, the rRNA operon is transcribed toward the SSC region in Nephroselmis and streptophyte cpDNAs. The orientation of the rRNA operon cannot be established in Chlamydomonas cpDNA owing to the extensively scrambled single copy regions, and this orientation remains unknown in Chlorella cpDNA because of the IR loss.
Considering that Oltmannsiellopsis and Pseudendoclonium represent distinct, early diverging lineages of the Ulvophyceae, the striking similarities between the quadripartite architectures of Oltmannsiellopsis and Pseudendoclonium cpDNAs suggest that both the atypical gene partitioning pattern and unusual orientation of the IR were characteristic of the chloroplast genome of earliest-diverging ulvophytes. Our data predict that the SSC region of the last common ancestor of Oltmannsiellopsis and Pseudendoclonium cpDNAs featured 12 of the genes usually found in the LSC region in Nephroselmis and streptophyte cpDNAs, whereas the LSC region contained exclusively genes characteristic of the ancestral LSC region. Consequently, in the lineage leading to Pseudendoclonium, two extra genes were transferred to the SSC region, whereas 40 additional genes migrated to this region in the Oltmannsiellopsis lineage. Although the mechanisms underlying these gene migrations between single copy regions remain unknown, they probably involved intramolecular or intermolecular recombination events. The analysis of conserved gene clusters reported below clearly indicates that several genes were transferred together in the course of these migrations.
Genes have been more extensively shuffled between the two single copy regions in Chlamydomonas cpDNA (Figure 1). It can be envisioned that during the evolution of ulvophytes and chlorophycean green algae, the ancestral pattern of gene partitioning was disrupted in successive steps, with a Pseudendoclonium-like organization evolving into an Oltmannsiellopsis-like organization, leading ultimately to the extensive scrambling of genes observed in Chlamydomonas. Given the absence of the IR from the Chlorella genome, it is very difficult to ascertain whether the transcription direction of the rRNA operon changed and whether genes were relocated from one genomic region to another during the evolution of trebouxiophytes. Loss of the IR is usually associated with many gene rearrangements ; in the case of Chlorella cpDNA, however, all the genes usually found in the ancestral SSC region have remained clustered, with the exception of three genes (psaC, ycf20 and trnL(uag)) (Figure 1). Investigations of IR-containing chloroplast genomes from distinct trebouxiophyte lineages will be required to test whether some of the gene relocations identified here in both Oltmannsiellopsis and Pseudendoclonium cpDNAs originated from the common ancestor of UTC algae.
Two ancestral clusters display breakpoints that are unique to the Ulvophyceae. The almost universally conserved psbB-psbT-psbN-psbH cluster was fragmented at the 5' end of psbN, creating two separate pieces, each encoding a pair of genes, in Oltmannsiellopsis cpDNA. In the Pseudendoclonium lineage, the introduction of an additional breakpoint on the opposite side of psbN led to the relocation of this gene on the DNA strand encoding psbB, psbT and psbH, without any change in gene order. In the Oltmannsiellopsis lineage, three breakpoints occurred in the ancestral rRNA operon to generate a new transcription unit in which the order of the trnA(ugc) and trnI(gau) genes has been reversed. Rearranged rRNA operons have been reported for the cpDNAs of the trebouxiophyte Chlorella ellipsoidea  and the ulvophyte Codium fragile ; however, in these cases, the ancestral rRNA operon was split into separate fragments that are transcribed from different promoters.
Minimal numbers of inversions accounting for gene rearrangements between green algal cpDNAs
Number of inversionsa
SDR units in Oltmannsiellopsis cpDNA
The SDRs in Oltmannsiellopsis cpDNA do not closely resemble those present in other UTC cpDNAs. The Oltmannsiellopsis repeats are biased in G+C, whereas the Chlorella repeats show a bias in A+T. The Pseudendoclonium and Chlamydomonas SDRs are also rich in G+C, but their sequences share no obvious similarities with the Oltmannsiellopsis repeats. This lack of sequence similarities between SDRs derived from distinct UTC genomes suggests that SDRs have been acquired independently in UTC lineages. However, the alternative hypothesis that SDRs were transmitted vertically cannot be excluded if we assume that these elements evolve at a very fast pace. Studies of cpDNAs from closely related UTC taxa will be required to distinguish between these two hypotheses.
Although the Oltmannsiellopsis chloroplast genome differs considerably from its Pseudendoclonium counterpart at the levels of intron content and gene order, the two ulvophyte genomes share similarities in gene content and quadripartite architecture. We conclude that the chloroplast genome of the last common ancestor of Oltmannsiellopsis and Pseudendoclonium contained a minimum of 108 genes, was loosely packed with coding sequences, carried only a few group I introns, and featured a quadripartite architecture that deviates from the ancestral type displayed by Mesostigma and Nephroselmis cpDNAs with regard to the transcription direction of the rRNA genes and the gene contents of the single copy regions. Given the phylogenetic positions of Oltmannsiellopsis and Pseudendoclonium, these genomic characters were undoubtedly present in the earliest-diverging members of the Ulvophyceae. Numerous changes were experienced by the chloroplast genome in the lineages leading to Oltmannsiellopsis and Pseudendoclonium; these include contraction/expansion of the IR, migration of genes from the ancestral LSC region toward the single copy region corresponding to the SSC, gene losses, intron gains/losses, and gene rearrangements within the IR and each of the single copy regions. Considering that the chloroplast genome of Codium fragile (Ulvales) is greatly reduced in size (only 89 kbp) and lacks an IR , many additional chloroplast gene losses and rearrangements probably occurred in some lineages of the Ulvophyceae.
Our comparative analysis of the Oltmannsiellopsis chloroplast genome with its chlorophyte counterparts strengthens the idea that the chloroplast genomes of early-diverging ulvophytes occupy an intermediate position between those of the trebouxiophyte Chlorella and the chlorophycean green alga Chlamydomonas with respect to the retention of ancestral features . In the context of the debate on the branching order of UTC lineages [4–6], this analysis provides further support for the published phylogenetic analysis of mitochondrial gene sequences identifying the Trebouxiophyceae as a basal lineage relative to the Ulvophyceae and Chlorophyceae .
Isolation and sequencing of OltmannsiellopsiscpDNA
Oltmannsiellopsis viridis was obtained from the National Institute for Environmental Studies of Japan (NIES 360) and grown in K medium  under 12 h light/dark cycles. Organellar DNA was isolated and sequenced as described previously . Sequences were edited and assembled with SEQUENCHER 4.2.1 (GeneCodes, Ann Arbor, MI). The fully annotated chloroplast genome sequence has been deposited in [GenBank:DQ291132].
Genes and ORFs were identified as described previously . Homologous introns were detected by BLASTN searches  against the non-redundant database of National Center for Biotechnology Information using an E value threshold of 1 × 10-4. Homologous introns inserted at identical positions within the same gene were identified by manual screening of the GOBASE database .
Repeated sequences were mapped with PipMaker , identified with REPuter 2.74  and classified with REPEATFINDER , using the default parameters. Sequences clustered with REPEATFINDER were aligned manually using BIOEDIT 7.0.1 , and non-overlapping SDR units were identified by manual screening of the alignment. Numbers of SDR units were determined with FINDPATTERNS of the GCG Wisconsin Package version 10.2 (Accelrys, Burlington, Mass.), using 100% or 90% sequence identity. Putative stem-loop structures and degenerate repeats were identified using PALINDROME and ETANDEM in EMBOSS 2.9.0 , respectively. The density of repeated elements in a given chloroplast genome was assessed with REPuter 2.74  using the -f (forward), -p (palindromic), and -allmax options at minimum lengths (-l) of 30 bp and 45 bp. For the analyses involving IR-containing genomes, one copy of the IR sequence was deleted. Circle graphs generated by REPuter were screen-captured at 300 dpi and converted to black and white illustrations with GIMP 2.0 . Repeated elements in different cpDNAs were compared using Vmatch  and GenAlyzer 0.81 b .
The GRIMM web server  was used to infer the minimal number of gene permutations by inversions in pairwise comparisons of chloroplast genomes. Because GRIMM cannot deal with duplicated genes and requires that the compared genomes have the same gene content, genes within one of the two copies of the IR were excluded and only the genes common to all the compared genomes were analysed. The data set used in the comparative analyses reported in Table 6 contained 90 genes; the three exons of the trans-spliced psaA gene were coded as distinct fragments (for a total of 92 gene loci).
large single copy
open reading frame
short dispersed repeat
small single copy
We are grateful to Charles O'Kelly for his valuable suggestions of candidate taxa for this study, to Patrick Charlebois for his help with the analysis of conserved gene clusters, and to Philippe Beauchamp for his technical assistance in determining the Oltmannsiellopsis cpDNA sequence. We also thank Christian Otis for critical reading of the manuscript. This work was supported by a grant from the Natural Sciences and Engineering Research Council of Canada (to MT and CL).
- Bremer K: Summary of green plant phylogeny and classification. Cladistics. 1985, 1: 369-385.View ArticleGoogle Scholar
- Sluiman HJ: The green algal class Ulvophyceae. An ultrastructural survey and classification. Crypt Bot. 1989, 1: 83-94.Google Scholar
- Lewis LA, McCourt RM: Green algae and the origin of land plants. Am J Bot. 2004, 91 (10): 1535-1556.View ArticlePubMedGoogle Scholar
- Friedl T, O'Kelly CJ: Phylogenetic relationships of green algae assigned to the genus Planophila (Chlorophyta): evidence from 18S rDNA sequence data and ultrastructure. Eur J Phycol. 2002, 37: 373-384. 10.1017/S0967026202003712.View ArticleGoogle Scholar
- Pombert JF, Otis C, Lemieux C, Turmel M: The complete mitochondrial DNA sequence of the green alga Pseudendoclonium akinetum (Ulvophyceae) highlights distinctive evolutionary trends in the Chlorophyta and suggests a sister-group relationship between the Ulvophyceae and Chlorophyceae. Mol Biol Evol. 2004, 21 (5): 922-935. 10.1093/molbev/msh099.View ArticlePubMedGoogle Scholar
- Pombert JF, Otis C, Lemieux C, Turmel M: The Chloroplast Genome Sequence of the Green Alga Pseudendoclonium akinetum (Ulvophyceae) Reveals Unusual Structural Features and New Insights into the Branching Order of Chlorophyte Lineages. Mol Biol Evol. 2005, 22 (9): 1903-1918. 10.1093/molbev/msi182.View ArticlePubMedGoogle Scholar
- Lemieux C, Otis C, Turmel M: Ancestral chloroplast genome in Mesostigma viride reveals an early branch of green plant evolution. Nature. 2000, 403 (6770): 649-652. 10.1038/35001059.View ArticlePubMedGoogle Scholar
- Turmel M, Ehara M, Otis C, Lemieux C: Phylogenetic relationships among Streptophytes as inferred from chloroplast small and large subunit rRNA gene sequences. J Phycol. 2002, 38: 364-375. 10.1046/j.1529-8817.2002.01163.x.View ArticleGoogle Scholar
- Turmel M, Otis C, Lemieux C: The complete mitochondrial DNA sequence of Mesostigma viride identifies this green alga as the earliest green plant divergence and predicts a highly compact mitochondrial genome in the ancestor of all green plants. Mol Biol Evol. 2002, 19 (1): 24-38.View ArticlePubMedGoogle Scholar
- Bhattacharya D, Weber K, An SS, Berning-Koch W: Actin phylogeny identifies Mesostigma viride as a flagellate ancestor of the land plants. J Mol Evol. 1998, 47 (5): 544-550. 10.1007/PL00006410.View ArticlePubMedGoogle Scholar
- Marin B, Melkonian M: Mesostigmatophyceae, a new class of streptophyte green algae revealed by SSU rRNA sequence comparisons. Protist. 1999, 150 (4): 399-417.View ArticlePubMedGoogle Scholar
- Karol KG, McCourt RM, Cimino MT, Delwiche CF: The closest living relatives of land plants. Science. 2001, 294: 2351-2353. 10.1126/science.1065156.View ArticlePubMedGoogle Scholar
- Turmel M, Otis C, Lemieux C: The chloroplast and mitochondrial genome sequences of the charophyte Chaetosphaeridium globosum: insights into the timing of the events that restructured organelle DNAs within the green algal lineage that led to land plants. Proc Natl Acad Sci USA. 2002, 99 (17): 11275-11280. 10.1073/pnas.162203299.PubMed CentralView ArticlePubMedGoogle Scholar
- Turmel M, Otis C, Lemieux C: The complete chloroplast DNA sequence of the green alga Nephroselmis olivacea: insights into the architecture of ancestral chloroplast genomes. Proc Natl Acad Sci USA. 1999, 96 (18): 10248-10253. 10.1073/pnas.96.18.10248.PubMed CentralView ArticlePubMedGoogle Scholar
- Palmer JD: Plastid chromosomes: structure and evolution. The Molecular Biology of Plastids Cell Culture and Somatic Cell Genetics of Plants. Edited by: Bogorad L, Vasil I. 1991, San Diego: Academic Press, 7A: 5-53.Google Scholar
- Goulding SE, Olmstead RG, Morden CW, Wolfe KH: Ebb and flow of the chloroplast inverted repeat. Mol Gen Genet. 1996, 252 (1–2): 195-206. 10.1007/BF02173220.View ArticlePubMedGoogle Scholar
- Wakasugi T, Nagai T, Kapoor M, Sugita M, Ito M, Ito S, Tsudzuki J, Nakashima K, Tsudzuki T, Suzuki Y, Hamada A, Ohta T, Inamura A, Yoshinaga K, Sugiura M: Complete nucleotide sequence of the chloroplast genome from the green alga Chlorella vulgaris: the existence of genes possibly involved in chloroplast division. Proc Natl Acad Sci USA. 1997, 94 (11): 5967-5972. 10.1073/pnas.94.11.5967.PubMed CentralView ArticlePubMedGoogle Scholar
- Maul JE, Lilly JW, Cui L, dePamphilis CW, Miller W, Harris EH, Stern DB: The Chlamydomonas reinhardtii plastid chromosome: islands of genes in a sea of repeats. Plant Cell. 2002, 14 (11): 2659-2679. 10.1105/tpc.006155.PubMed CentralView ArticlePubMedGoogle Scholar
- Chihara M, Inouye I, Takahata N: Oltmannsiellopsis, a new genus of marine flagellate (Dunaliellaceae, Chlorophyceae). Arch Protistenkd. 1986, 132: 313-324.View ArticleGoogle Scholar
- Lokhorst GM, Star W: The flagellar apparatus in the marine flagellate algal genus Oltmannsiellopsis (Dunaliellales, Chlorophyceae). Arch Protistenkd. 1993, 143: 13-32.View ArticleGoogle Scholar
- Hargraves PE, Steele RL: Morphology and ecology of Oltmannsiella virida, sp. nov. (Chlorophyceae: Volvocales). Phycologia. 1980, 19: 96-102.View ArticleGoogle Scholar
- Nakayama T, Watanabe S, Inouye I: Phylogeny of wall-less green flagellates inferred from 18S rDNA sequence data. Phycological Research. 1996, 44: 151-161. 10.1111/j.1440-1835.1996.tb00044.x.View ArticleGoogle Scholar
- O'Kelly CJ, Wysor B, Bellows WK: Gene sequence diversity and the phylogenetic position of algae assigned to the genera Phaeophila and Ochlochaete (Ulvophyceae, Chlorophyta). J Phycol. 2004, 40: 789-799. 10.1111/j.1529-8817.2004.03204.x.View ArticleGoogle Scholar
- O'Kelly CJ, Wysor B, Bellows WK: Collinsiella (Ulvophyceae, Chlorophyta) and other ulotrichalean taxa with shell-boring sporophytes form a monophyletic clade. Phycologia. 2004, 43 (1): 41-49.View ArticleGoogle Scholar
- O'Kelly CJ, Bellows WK, Wysor B: Phylogenetic position of Bolbocoleon piliferum (Ulvophyceae, Chlorophyta): Evidence from reproduction, zoospore and gamete ultrastructure, and small subunit rRNA gene sequences. J Phycol. 2004, 40: 209-222. 10.1111/j.1529-8817.2004.03204.x.View ArticleGoogle Scholar
- Yamada T, Shimaji M: Splitting of the ribosomal RNA operon on chloroplast DNA from Chlorella ellipsoidea. Mol Gen Genet. 1987, 208 (3): 377-383. 10.1007/BF00328127.View ArticleGoogle Scholar
- Manhart JR, Kelly K, Dudock BS, Palmer JD: Unusual characteristics of Codium fragile chloroplast DNA revealed by physical and gene mapping. Mol Gen Genet. 1989, 216 (2–3): 417-421. 10.1007/BF00334385.View ArticlePubMedGoogle Scholar
- Boudreau E, Turmel M: Gene rearrangements in Chlamydomonas chloroplast DNAs are accounted for by inversions and by the expansion/contraction of the inverted repeat. Plant Mol Biol. 1995, 27 (2): 351-364. 10.1007/BF00020189.View ArticlePubMedGoogle Scholar
- Boudreau E, Turmel M: Extensive gene rearrangements in the chloroplast DNAs of Chlamydomonas species featuring multiple dispersed repeats. Mol Biol Evol. 1996, 13 (1): 233-243.View ArticlePubMedGoogle Scholar
- Cosner ME, Raubeson LA, Jansen RK: Chloroplast DNA rearrangements in Campanulaceae: phylogenetic utility of highly rearranged genomes. BMC Evol Biol. 2004, 4 (1): 27-10.1186/1471-2148-4-27.PubMed CentralView ArticlePubMedGoogle Scholar
- Milligan BG, Hampton JN, Palmer JD: Dispersed repeats and structural reorganization in subclover chloroplast DNA. Mol Biol Evol. 1989, 6 (4): 355-368.PubMedGoogle Scholar
- Keller MD, Selvin RC, Claus W, Guillard RRL: Media for the culture of oceanic ultraphytoplankton. J Phycol. 1987, 23: 633-638.View ArticleGoogle Scholar
- Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ: Basic local alignment search tool. J Mol Biol. 1990, 215 (3): 403-410. 10.1006/jmbi.1990.9999.View ArticlePubMedGoogle Scholar
- O'Brien EA, Badidi E, Barbasiewicz A, deSousa C, Lang BF, Burger G: GOBASE – a database of mitochondrial and chloroplast information. Nucleic Acids Res. 2003, 31 (1): 176-178. 10.1093/nar/gkg090.PubMed CentralView ArticlePubMedGoogle Scholar
- Schwartz S, Zhang Z, Frazer KA, Smit A, Riemer C, Bouck J, Gibbs R, Hardison R, Miller W: PipMaker – a web server for aligning two genomic DNA sequences. Genome Res. 2000, 10 (4): 577-586. 10.1101/gr.10.4.577.PubMed CentralView ArticlePubMedGoogle Scholar
- Kurtz S, Choudhuri JV, Ohlebusch E, Schleiermacher C, Stoye J, Giegerich R: REPuter: the manifold applications of repeat analysis on a genomic scale. Nucleic Acids Res. 2001, 29 (22): 4633-4642. 10.1093/nar/29.22.4633.PubMed CentralView ArticlePubMedGoogle Scholar
- Volfovsky N, Haas BJ, Salzberg SL: A clustering method for repeat analysis in DNA sequences. Genome Biol. 2001, 2 (8): Research0027-10.1186/gb-2001-2-8-research0027.PubMed CentralView ArticlePubMedGoogle Scholar
- Hall TA: BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp Ser. 1999, 41: 95-98.Google Scholar
- Rice P, Longden I, Bleasby A: EMBOSS: the European Molecular Biology Open Software Suite. Trends Genet. 2000, 16 (6): 276-277. 10.1016/S0168-9525(00)02024-2.View ArticlePubMedGoogle Scholar
- The GNU Image Manipulation Program. [http://www.gimp.org]
- The Vmatch large scale analysis software. [http://www.vmatch.de]
- Choudhuri JV, Schleiermacher C, Kurtz S, Giegerich R: GenAlyzer: interactive visualization of sequence similarities between entire genomes. Bioinformatics. 2004, 20 (12): 1964-1965. 10.1093/bioinformatics/bth161.View ArticlePubMedGoogle Scholar
- Tesler G: GRIMM: genome rearrangements web server. Bioinformatics. 2002, 18 (3): 492-493. 10.1093/bioinformatics/18.3.492.View ArticlePubMedGoogle Scholar
- Michel F, Westhof E: Modelling of the three-dimensional architecture of group I catalytic introns based on comparative sequence analysis. J Mol Biol. 1990, 216 (3): 585-610. 10.1016/0022-2836(90)90386-Z.View ArticlePubMedGoogle Scholar
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