- Research article
- Open Access
EST analysis of the scaly green flagellate Mesostigma viride (Streptophyta): Implications for the evolution of green plants (Viridiplantae)
- Andreas Simon†1,
- Gernot Glöckner†2,
- Marius Felder2,
- Michael Melkonian1 and
- Burkhard Becker1Email author
© Simon et al; licensee BioMed Central Ltd. 2006
- Received: 31 October 2005
- Accepted: 13 February 2006
- Published: 13 February 2006
The Viridiplantae (land plants and green algae) consist of two monophyletic lineages, the Chlorophyta and the Streptophyta. The Streptophyta include all embryophytes and a small but diverse group of freshwater algae traditionally known as the Charophyceae (e.g. Charales, Coleochaete and the Zygnematales). The only flagellate currently included in the Streptophyta is Mesostigma viride Lauterborn. To gain insight into the genome evolution in streptophytes, we have sequenced 10,395 ESTs from Mesostigma representing 3,300 independent contigs and compared the ESTs of Mesostigma with available plant genomes (Arabidopsis, Oryza, Chlamydomonas), with ESTs from the bryophyte Physcomitrella, the genome of the rhodophyte Cyanidioschyzon, the ESTs from the rhodophyte Porphyra, and the genome of the diatom Thalassiosira.
The number of expressed genes shared by Mesostigma with the embryophytes (90.3 % of the expressed genes showing similarity to known proteins) is higher than with Chlamydomonas (76.1 %). In general, cytosolic metabolic pathways, and proteins involved in vesicular transport, transcription, regulation, DNA-structure and replication, cell cycle control, and RNA-metabolism are more conserved between Mesostigma and the embryophytes than between Mesostigma and Chlamydomonas. However, plastidic and mitochondrial metabolic pathways, cytoskeletal proteins and proteins involved in protein folding are more conserved between Mesostigma and Chlamydomonas than between Mesostigma and the embryophytes.
Our EST-analysis of Mesostigma supports the notion that this organism should be a suitable unicellular model for the last flagellate common ancestor of the streptophytes. Mesostigma shares more genes with the embryophytes than with the chlorophyte Chlamydomonas reinhardtii, although both organisms are flagellate unicells. Thus, it seems likely that several major physiological changes (e.g. in the regulation of photosynthesis and photorespiration) took place early during the evolution of streptophytes, i.e. before the transition to land.
- Calvin Cycle
- Terrestrial Habitat
- Average Identity
- Arginine Kinase
- Glycolate Oxidase
The Viridiplantae (literally meaning green plants) include all green algae and embryophyte plants. They represent a monophyletic group of organisms, which display a surprising diversity with respect to their morphology, cell architecture, life histories and reproduction, and their biochemistry. The colonization of the terrestrial habitat by streptophyte algae 450 – 470 million years ago [reviewed in ] was undoubtedly one of the most important steps in the evolution of life on earth [2–4], which paved the way for the evolution of the various groups of land plants (embryophytes = bryophytes, pteridophytes and spermatophytes) resulting in our current terrestrial ecosystems .
A thorough understanding of the evolution of land plants requires knowledge about the phylogeny of green algae and embryophytes as well as insight into the evolution of plant genomes with special reference to developmental processes. Whereas our knowledge about the phylogeny of the Viridiplantae has greatly increased over the last years, the latter has hardly been addressed to date.
The Viridiplantae are grouped into two divisions: the Chlorophyta and the Streptophyta . The Chlorophyta comprise the vast majority of green algae including most scaly green flagellates (e.g. Pyramimonas, Tetraselmis), the Ulvophyceae (e.g. Ulva, Acetabularia), Chlorophyceae (e.g. Chlamydomonas, Volvox) and Trebouxiophyceae (e.g. Chlorella) [7, 8]. The Streptophyta include all embryophyte plants and a diverse paraphyletic assemblage of freshwater green algae, the Charales (stoneworts), Coleochaete, the Zygnematophyceae and a few other taxa . Currently, the Charales are thought to be the sister group of the embryophytes suggesting that the evolution of true land plants already started with a complex organism . Remarkably, only a single scaly green flagellate Mesostigma viride Lauterborn, has been found to belong to the Streptophyta [10–13]. The exact phylogenetic position of Mesostigma viride, however, is still controversial [10–12, 14–16]. Mesostigma has recently attracted much attention as a putative key organism for the understanding of the early evolution of the Streptophyta [17–20].
Two aspects in the evolution of land plants seem to be important in this respect. First, many key evolutionary inventions of plants took already place within the streptophyte algae. According to Graham et al.  one can distinguish several major transitions in the evolution of land plants starting with a Mesostigma-like flagellate ancestor: development of a cellulosic cell wall, multicellularity, cytokinesis by a phragmoplast, plasmodesmata, apical meristematic cell and apical cell proliferation leading to branching, asymmetric cell division, cell differentiation, retention of zygotes, heteromorphic life history, and a root meristem. Of these distinguishing features only the latter two evolved not until the embryophytes emerged. Second, the colonization of the terrestrial habitat with its exposure to air, increased solar radiation and life in a desiccating environment led to adaptations of cell architecture, metabolism and body plan to survive in the terrestrial ecosystems . The evolutionary history of these adaptations is currently not known. Important questions are: How did the green algal progenitor adapt to the terrestrial habitat? Which genomic changes were associated with this transition? And which of these genes are derived from streptophyte green algae? To gain insight into these questions we have started to analyze ESTs from various streptophyte algal lineages.
Here, we present an analysis of 10,395 ESTs representing 3306 non-redundant expressed genes obtained from Mesostigma viride. We show that the number of genes shared is higher between Mesostigma and the embryophytes than between Mesostigma and Chlamydomonas. Comparison of expressed genes from Mesostigma with the genomes of Arabidopsis, Chlamydomonas, the red alga Cyanidioschyzon, and rice as well as ESTs from Physcomitrella and Porphyra allowed us to identify conserved and derived cellular functions within the different evolutionary lines and to obtain a first insight into the metabolic capabilities of the flagellate ancestor of green plants.
Preparation and characterization of libraries
Mesostigma viride cDNA libraries used.
Number of primary clones
Percentage recombinant clones
size of inserts1 (bp)
average size of inserts1 (bp)
number of ESTs sequenced
small size fraction
large size fraction
total cDNA normalized
large size fraction normalized
2403 cDNAs = 4806 ESTs2
Initially, about 100–500 ESTs were sequenced from all libraries and analyzed by BLASTX against the Swissprot and translated Genbank databases. Since the Meso 2 and 4 libraries containing the larger inserts gave more promising results, we subsequently sequenced about 4000 additional ESTs from the Meso 2 and Meso 4 libraries, respectively yielding a total of 10,395 reads (5,527,413 bp). Based on comparison with published sequences from Mesostigma viride the rate of sequencing error was determined to be generally between 1% and 7 % (average 4 %) depending on the quality of the sequence.
Summary of Mesostigma viride expressed genes obtained from four cDNA libraries (Meso 1 – Meso 4).
No of contigs
with recognizable protein motif
no protein motifs
with known function3
Functional classification of 3006 Mesostigma viride contigs using the KOG system  and an expectation threshold of e = 10-7.
No. of Contigs
INFORMATION STORAGE AND PROCESSING
[J] Translation, ribosomal structure and biogenesis
[A] RNA processing and modification
[L] Replication, recombination and repair
[B] Chromatin structure and dynamics
CELLULAR PROCESSES AND SIGNALING
[D] Cell cycle control, cell division, chromosome partitioning
[Y] Nuclear structure
[V] Defense mechanisms
[T] Signal transduction mechanisms
[M] Cell wall/membrane/envelope biogenesis
[N + Z] Cytoskeleton and cell motility
[W] Extracellular structures
[U] Intracellular trafficking, secretion, and vesicular transport
[O] Posttranslational modification, protein turnover, chaperones
[C] Energy production and conversion
[G] Carbohydrate transport and metabolism
[E] Amino acid transport and metabolism
[F] Nucleotide transport and metabolism
[H] Coenzyme transport and metabolism
[I] Lipid transport and metabolism
[P] Inorganic ion transport and metabolism
[Q] Secondary metabolites biosynthesis, transport and catabolism
[R] General function prediction only
[S] Function unknown
[X] Unnamed protein
Classification of MesostigmaESTs according to homologous genes in other organisms
Overall protein similarities between various photoautotrophic organisms
Comparison of the Mesostigma expressed genes with the genomes and ESTs from various organisms. Average identity (AI) of pair wise comparisons of Mesostigma expressed genes with the indicated organismal data set.
Data set (No. of contigs)
0.653 (n = 244)1)
0.585 (n = 188)1)
0.675 (n = 301)1)
Evolutionary distance D2)
The AI between Mesostigma and Chlamydomonas or the embryophytes are very similar. The highest AI value obtained was for Physcomitrella/Mesostigma followed by Arabidopsis/Mesostigma, Chlamydomonas/ Mesostigma and Oryza/Mesostigma. The full data set includes many proteins, which we detected only in some species using Mesostigma expressed genes as a query. Therefore, we constructed a constrained data set (314 expressed genes, including at least 46 nuclear encoded plastidic, 9 nuclear encoded mitochondrial, and 73 cytosolic ribosomal proteins), containing only Mesostigma genes which gave matches with all completed genomes from photoautotrophic eukaryotic organisms (including the diatom Thalassiosira). This constrained data set represents a conserved core set of nuclear encoded expressed proteins from photoautotrophic eukaryote organisms. We calculated AI values for the constrained data set using complete genomes and the available ESTs of Physcomitrella, Porphyra, and Chlamydomonas. The results are included in Table 4. We obtained the highest AI-values in the constrained data set for the three embryophytes, followed by Chlamydomonas. The similar AI values for the three different embryophytes suggest that the overall evolutionary rate was very similar for the embryophytes investigated, when compared with Mesostigma (see below).
Statistical significance of the obtained AI values. A paired students t-test was performed for the constrained data set to test whether the observed differences between the average identity of pair wise comparisons of Mesostigma expressed genes with the indicated organismal data set are significant. Differences are considered significant when p is < 0.0071 (0.05/8 Bonferroni adjustment ).
No. of genes shared2
Degrees of freedom
Mesostigma/Chlamydomonas G Mesostigma/Chlamydomonas E
Mesostigma/Chlamydomonas G Mesostigma/Physcomitrella E
Mesostigma/Chlamydomonas G Mesostigma/Arabidopsis G
Mesostigma/Chlamydomonas G Mesostigma./Oryza G
Mesostigma/Physcomitrella E Mesostigma/Arabidopsis G
Mesostigma/Physcomitrella E Mesostigma./Oryza G
Mesostigma/Arabidopsis G Mesostigma./Oryza G
Two other results are remarkable. First, for the calculation of the AI it is possible to use large EST-data sets instead of genomes. We obtained the same result for Mesostigma/Chlamydomonas genome and for Mesostigma/Chlamydomonas ESTs (AI = 0.653 for both data sets; p = 0,975, Table 5, using 244 expressed genes from Mesostigma). Similarly, when Mesostigma/Physcomitrella ESTs were compared with the Mesostigma/Arabidopsis genome and with the Mesostigma/Oryza genome only small differences were observed (AI = 0,675/0,681; 0,675/0,673 respectively, using 302 expressed genes from Mesostigma, Table 5). Statistical analysis (paired students t-test) showed that the observed differences are not significant. Furthermore, we note that the genome of the diatom Thalassiosira pseudonana shows a similar AI in respect to Mesostigma as the red algal genome and ESTs (Table 4). The difference values of these distantly related genomes represent presumably an upper threshold for reasonable AI value calculations.
Analysis of metabolic pathways
ESTs have been widely used for the identification of metabolic pathways . A complete list of all metabolic pathways identified is presented in supplemental Table 2 [see Additional file 2]. Indeed, many ESTs showed similarity to proteins required for photosynthesis (66 expressed genes), nucleotide synthesis (6), nucleotide sugar conversion, the biosynthesis of precursors of scale polysaccharides (6), heme and chlorophyll biosynthesis (6), fatty acid and lipid biosynthesis (9), terpenoid biosynthesis (6), glycolysis (11) and the TCA-cycle including pyruvate dehydrogenase and respiration (12). The biosynthetic pathways for several amino acids were also well represented in our ESTs (21 expressed genes for Ala, Arg, Gly, Ile, Leu, Lys, Pro, Ser, Thr, Trp and Val). However, for several other amino acids (Asn, Asp, Cys, Gln, Glu, His, Met, Phe, Tyr) we did not find a single EST which could be matched to the known biosynthetic pathways.
A total of 25 expressed genes encode components of the light-harvesting complex. There are some light-harvesting complex proteins, which Mesostigma shares only with the chlorophytes and red algae (e.g. so called fucoxanthin/chlorophyll a-binding proteins). For others, we detected similar proteins only within embryophytes. However, the lhc proteins form a large superfamily and their phylogenetic analysis is beyond the scope of this study.
Several genes encode proteins of the photorespiratory C2-cycle (glycolate phosphatase, peroxisomal glycolate oxidase, a component of the glycine decarboxylase enzyme complex, and a peroxisomal serine-glyoxylate transaminase). As in embryophytes, the NADH required for reduction of hydroxy pyruvate is produced by a peroxisomal NADH malate dehydrogenase.
We did not find evidence for a hexokinase and sucrose biosynthesis in interphase cells of Mesostigma. Several ESTs represent plastidic pyruvate kinase, however, only a single EST coded for the cytosolic isoform. Expressed genes for PEP carboxylase and a cytosolic malate dehydrogenase are present, suggesting that malate may be the major substrate for respiration in the mitochondrion of Mesostigma as in many embryophytes. The plastidic pyruvate kinase probably functions in the generation of acetyl-CoA required to sustain fatty acid synthesis in plastids.
Scales consist mainly of the 2-keto sugar acids 3-deoxy-manno-octulosonic acid (2-keto-3-deoxy-oktonate, kdo), 5OMekdo, 3-deoxy-lyxo-heptulosaric acid, dha) and gal, galA, gul and some minor monosaccharides . Expressed genes coding for kdo synthesis, and activation of kdo as CMP-kdo are present. The obtained sequence similar to a CMP-sialA transporter might actually be the CMP-kdo transporter necessary for uptake of CMP-kdo into the Golgi apparatus, as kdo and sialA are structural analogs. Interestingly, kdo-synthase and CMP-kdo-transferase are among the most conserved proteins between Mesostigma and the embryophytes. As in embryophytes , galA is synthesized via the UDP-glc dehydrogenase pathway and the myo-inositol oxygenase pathway. We could not detect the latter enzyme in Chlamydomonas or red algae.
Our EST-data support the presence of vitamin B12-biosynthesis and the production of a phosphagen phosphoarginine by arginine kinase in Mesostigma.
Evolution of metabolism and cell structure
Comparison of Mesostigma genes related to metabolic functions with Chlamydomonas and three embryophytes. The average identity (AI) of pair-wise comparisons of Mesostigma expressed genes coding for the indicated metabolic function with the ESTs or genome of the given organisms are presented.
Plastidic metabolism (107)2
Mitochondrial metabolism (16)2
cytosolic metabolism (glycolysis, NDP-sugar metabolism, nucleotide synthesis, 22)2
Comparison of Mesostigma genes related to cell structure functions with the genome or ESTs of Chlamydomonas and three embryophytes. The average identity of pair-wise comparisons of Mesostigma expressed genes coding for the indicated cellular functions with the ESTs or genomes of the given organisms are presented.
Cell structure (201)
Protein folding/Chaperones (21)
Cytosolic protein degradation (22)
Vesicular transport (22)
DNA structure, replication, cell cycle (21)
RNA metabolism (23)
In this study, we have analyzed about 3000 expressed genes from the scaly green flagellate Mesostigma viride. We compared the expressed genes with the complete genomes from the angiosperms Arabidopsis thaliana and Oryza sativa, the chlorophyte Chlamydomonas reinhardtii, the red alga Cyanidioschyzon merolae and the diatom Thalassiosira pseudonana, as well as the ESTs from the moss Physcomitrella patens, and the red alga Porphyra yezoensis. Altogether, the Mesostigma proteome is more similar to the embryophytes than to Chlamydomonas, although Mesostigma and Chlamydomonas are both flagellate unicells. Mesostigma shares more genes with the embryophytes than with Chlamydomonas, including several enzymes confined to the streptophytes (e.g. GAPDH B, [Cu-Zn] superoxide dismutase), and the average identity of shared proteins is higher between Mesostigma and the embryophytes than between Mesostigma and Chlamydomonas. Therefore, we consider Mesostigma to be a member of the streptophytes, although Mesostigma clearly shares some ancestral characters with chlorophytes. Plastidic (with the exception of the Calvin cycle) and mitochondrial functions e.g. seem to be more conserved between Mesostigma and chlorophytes than between Mesostigma and embryophytes, i.e. these functions are more derived in embryophytes, probably due to adaptation of embryophytes to the terrestrial habitat. In contrast, other cellular functions except for the cytoskeleton are more conserved between Mesostigma and embryophytes than between Mesostigma and Chlamydomonas. Interestingly, in previous phylogenetic analyses plastidic and mitochondrial genes failed to show a clear relationship between Mesostigma and the streptophytes [14, 15], whereas actin and nuclear-encoded SSU rDNA phylogenies support the notion that Mesostigma is a member of the streptophytes [10–12]. The different evolutionary rates for different cellular functions observed in this study might explain this discrepancy.
We calculated the average identity (AI) values from automatically generated BLAST output alignments. Automatically derived alignments are prone to errors. However, we believe that our approach is justified for the following reasons: (1) the BLAST alignments cover only the conserved parts of proteins and our calculated AI values indicate that in most alignments more than half of the amino acids are identical enhancing the quality of the automatically produced alignments; (2) although small mistakes may occur, they are insignificant given the high number of amino acids used to calculate the AI. On average the BLAST alignments contained about 150 amino acids and therefore about 45,000 amino acid positions were used in the constrained data set. In large data sets small unbiased errors become irrelevant . Our results indicate that at least 100 (better are 150–200) expressed genes have to be used to obtain statistically significant results. It could be argued that our analysis uses only similarity values and no real evolutionary distances. AI values can be easily converted into evolutionary distances using an approximation given by Kimura , with the effect that the differences between the various organisms become larger but no changes occur in the order of relatedness (included in Table 4). We conclude that the AI of proteins shared between different organisms represents a reasonable measure of evolutionary relatedness, if sufficiently large data sets are used.
In the following, we briefly discuss some major differences in coding potential observed between the different photosynthetic eukaryotic organisms.
11 of 18 proteins included in supplemental Table 1 [see Additional file 1] which are shared only by Mesostigma and Chlamydomonas are associated with flagellar functions such as axonemal dyneins or components of the IFT (intra-flagellar transport) machinery. Most likely, the angiosperms lost these proteins during evolution together with the ability to produce flagellate cells. The absence of these proteins in the ESTs from the moss Physcomitrella, is presumably due to the fact that ESTs from developing spermatozoids are not available.
Proteins shared by Mesostigma and the embryophytes but not present in chlorophytes perform diverse functions. There are some well known biochemical differences between chlorophytes and streptophytes such as the presence of (Cu-Zn) superoxide dismutase [29, 30] and glycolate oxidase in streptophytes [31, 32] but not in chlorophytes. In addition, streptophytes use the DXP and mevalonate pathways for isoprene biosynthesis whereas chlorophytes posses only the DXP pathway . For all these functions, we find molecular support in our expressed gene data set except for the mevalonate pathway of isoprene biosynthesis. Two genes matched two different enzymes of the DXP pathway; however, no matches for the MVA pathway were obtained, although the presence of this pathway has been demonstrated biochemically . This could be due to the selective expression of one or the other pathway under different environmental conditions.
Remarkably, our list of proteins uniquely shared by Mesostigma and the embryophytes includes several proteins involved in steroid biosynthesis (e.g. a 3-oxo-5-beta-steroid dehydrogenase and a C-4 sterol oxidase), a homeobox protein of the knox family and proteins of the F-box family. The latter protein family underwent a dramatic expansion in the embryophytes (Arabidopsis has more than 700 members of this family).
Our expressed protein data set contains sequences similar to a protein involved in vitamin B-12 metabolism (present in rhodophytes and chlorophytes), an arginine kinase and a ARL6 protein, the latter two are absent in chlorophytes, embryophytes and red algae. It has been shown that arginine kinase is part of the ATP regeneration system in cilia of Paramecium . Chlamydomonas lacks arginine kinase and recently Pazour et al.  showed that enzymes of the late glycolytic pathway are present in the flagella of Chlamydomonas, suggesting that the ATP required for flagellar function is produced by the glycolytic pathway in Chlamydomonas. The ARL6 protein has been implicated in protein translocation at the rER , although its exact function is still not known.
There are some typical embryophyte pathways that we failed to detect in Mesostigma, e.g. sucrose metabolism, hexokinase, and enzymes of cellulose biosynthesis. There are no reports about the presence of sucrose metabolism and hexokinase in green algae in the literature, whereas embryophyte-like Ces genes (catalytical subunit of cellulose synthase) have been reported in the streptophyte alga Mesotaenium . Although we cannot exclude that Mesostigma lost these genes, we do expect to find theses genes in the genome of Mesostigma.
Evolution of photosynthesis and photorespiration
It is well known that embryophytes and chlorophytes differ in important aspects of photosynthesis and its regulation, and in photorespiration (e.g., presence of GAPDHB, number of enzymes regulated by thioredoxin, glycolate oxidase vs. glycolate dehydrogenase, and presence or absence of (Cu-Zn) superoxide dismutase).
Regulation of plastidic enzymes by the thioredoxin system. Proteins similar to embryophyte plastidic thioredoxin-regulated proteins were identified in the genomes of Cyanidioschyzon, Chlamydomonas, and the ESTs of Mesostigma using the BLASTP or BLASTX algorithms. A putative thioredoxin-regulated orthologue as revealed by the conserved cysteine residues is indicated with +. An asterisk indicates putative cyanobacterial/plastidic proteins, which do not contain the conserved cysteines required for thioredoxin-regulation. Missing enzymes are indicated with -.
In summary, our EST analysis shows that Mesostigma shares more genes with the embryophytes than with the chlorophyte Chlamydomonas reinhardtii, although both organisms are flagellate unicells. Thus, it seems likely that many typical biochemical characteristics of streptophytes evolved early during the evolution of streptophytes, i.e. before the transition to land. Alternatively, such characteristics may haven been lost in the chlorophyte lineage or remain to be discovered in other chlorophytes. A decision between these alternatives requires further information on the genomes of other preferentially early branching chlorophytes such as Pyramimonas.
Our EST-analysis of Mesostigma supports the notion that this organism should be a suitable unicellular model for the last flagellate common ancestor of the streptophytes.
Plant material, RNA preparation and construction of libraries
Total RNA was isolated from cultures of Mesostigma viride Lauterborn (strain NIES 476, Tsukuba, Japan) and mRNA isolated using the mTRAP™ Total Kit (Active Motif). 5 μg of mRNA were converted into cDNA using the SuperScript™ Plasmid System (Invitrogen) and the cDNA obtained was fractionated by column chromatography. A large and a small size fraction were cloned into the pSPORT1 vector (Invitrogen).
Normalized full-length cDNA was prepared by Evrogen JSC (Moscow, Russia). cDNA was prepared from total RNA using the SMART approach  normalized using the DSN normalization method  and then amplified by PCR. cDNAs were either directly cloned into a pPCR-Script Amp SK(+) Vector (PCR-Script Amp Cloning Kit, Stratagene) or a large size fraction was isolated by column chromatography and then cloned into a pGEM-T Easy vector (Promega). All libraries were transformed into TOP 10 E. coli cells (Invitrogen) by electroporation.
Sequencing, contig assembly and data analysis
Clone preparation and sequencing
Isolated plasmids were sequenced by the cycle sequencing method using an ABI3700 96 capillary sequencer. A minimal contig set was assembled using the phrap assembler and all contigs were manually curated.
Each contig was compared as 3-frame translations to the protein databases Swissprot and genpept using blastx. Furthermore, all contigs were compared using the tBLASTX search algorithm to the genome sequence of Chlamydomonas reinhardtii, Cyanidioschyzon merolae, Thalassiosira pseudonana, Arabidopsis thaliana, Oryza sativa and to the EST databases of Physcomitrella patens and Porphyra yezoensis. The results were compiled to an Excel compatible file. Analyses of COG and KOG categories [43, 44] and Interpro protein domains  for the contigs were also performed.
Analysis of metabolic pathways
Using the metabolic pathways present at the AraCyc website , we identified all expressed genes with significant similarity to Arabidopsis genes present in AraCyc. Expressed genes that showed no significant similarity to Arabidopsis genes but to enzymes from other organisms were assigned to a pathway using the MetaCyc database .
Phylogenetic analysis of glycolate oxidase
Thirteen glycolate oxidase/lactate dehydrogenase sequences were obtained from public databases (Cyanidioschyzon merolae [KEGG:CMQ436C]; Chlamydomonas reinhardtii [JGI:C_340068]; Spinacia oleracea [Swiss-Prot:P05414]; Nostoc punctiforme PCC 73102 [Genbank:ZP_00106740.1]; Nostoc sp. PCC 7120 [Genbank:BAB77694.1]; Anabaena variabilis ATCC 29413 [Genbank:ZP_00160276.2]; Arabidopsis thaliana [Genbank:CAB78838], Oryza sativa [Genbank:AAB82143], Nicotiana tabacum [Genbank:AAC33509], Homo sapiens [Genbank:CAC34364], Drosophila melanogaster [Genbank:AAO41411], Dictyostelium discoideum [Genbank:XP_629946], Lactobacillus johnsonii NCC 533 [Genbank:NP_965805]). The nearly complete Mesostigma glycolate oxidase sequence was obtained by complete sequencing of EST clone Meso2b12b08. The sequences were aligned using Clustal X. The alignment was checked manually. Phylogenetic analyses were performed using the Phylip (neighbour joining and parsimony method) and MRBAYES software v 3.0 (Bayesian inference).
Sequence data from this article have been deposited with the EMBL/Genbank data libraries under accession numbers DN254242 to DN264595.
This work was supported by the DFG (Be1779/7-1).
- Sanderson MJ, Thorne JL, Wikstrom N, Bremer K: Molecular evidence on plant divergence times. Am J Bot. 2004, 91: 1656-1665.PubMedView ArticleGoogle Scholar
- Bateman RM, Crane PR, DiMichele WA, Kenrick PR, Rowe NP, Speck T, Stein WE: Early evolution of land plants: Phylogeny, physiology, and ecology of the primary terrestrial radiation. Annu Rev Ecol Syst. 1998, 29: 263-292. 10.1146/annurev.ecolsys.29.1.263.View ArticleGoogle Scholar
- Kenrick P, Crane PR: The origin and early diversification of land plants. 1997, Washington, London: Smithsonian Institution PressGoogle Scholar
- Graham LE: Origin of Land Plants. 1993, New York: John Wiley & Sons, IncGoogle Scholar
- Waters ER: Molecular adaptation and the origin of land plants. Molecular Phylogenetics and Evolution. 2003, 29: 456-463. 10.1016/j.ympev.2003.07.018.PubMedView ArticleGoogle Scholar
- Bremer K: Summary of green plant phylogeny and classification. Cladistics. 1985, 1: 369-385.View ArticleGoogle Scholar
- Mattox KR, Stewart KD: Classification of green algae: A concept based on comparative cytology. Systematics of the green algae. Edited by: Irvine DEG, John DM. 1984, London: Academic Press, 29-72.Google Scholar
- Nakayama T, Marin B, Kranz HD, Surek B, Huss VAR, Inouye I, Melkonian M: The basal position of scaly green flagellates among the green algae (Chlorophyta) is revealed by analyses of nuclear-encoded SSU rRNA sequences. Protist. 1998, 149: 367-380.PubMedView ArticleGoogle Scholar
- Huss VAR, Kranz HD: Charophyte evolution and the origin of land plants. Plant Syst Evol. 1997, 103-114.Google 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.PubMedView ArticleGoogle 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: 544-550. 10.1007/PL00006410.PubMedView ArticleGoogle Scholar
- Marin B, Melkonian M: Mesostigmatophyceae, a new class of streptophyte green algae revealed by SSU rRNA sequence comparisons. Protist. 1999, 150: 399-417.PubMedView ArticleGoogle Scholar
- Melkonian M, Marin B, Surek B: Phylogeny and Evolution of the Algae. Biodiversity and Evolution. Edited by: Arai R, Kato M, Doi Y. 1995, Tokyo: The National Science Museum Foundation, 153-176.Google 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: 24-38.PubMedView ArticleGoogle Scholar
- Lemieux C, Otis C, Turmel M: Ancestral chloroplast genome in Mesostigma viride reveals an early branch of green plant evolution. Nature. 2000, 403: 649-652. 10.1038/35001059.PubMedView ArticleGoogle Scholar
- Delwiche CF, Karol KG, Cimino MT, Sytsma KJ: Phylogeny of the genus Coleochaete (Coleochaetales, Charophyta) and related taxa inferred by analysis of the chloroplast gene rbcL. J Phycol. 2002, 38: 394-403. 10.1046/j.1529-8817.2002.01174.x.View ArticleGoogle Scholar
- Poethig RS: Life with 25,000 genes. Genome Res. 2001, 11: 313-316. 10.1101/gr.180001.PubMedView ArticleGoogle Scholar
- Palmer JD, Soltis DE, Chase MW: The plant tree of life: An overview and some points of view. Am J Bot. 2004, 91: 1437-1445.PubMedView ArticleGoogle Scholar
- Lewis LA, McCourt RM: Green algae and the origin of land plants. American Journal of Botany. 2004, 91: 1535-1556.PubMedView ArticleGoogle Scholar
- McCourt RM, Delwiche CF, Karol KG: Charophyte algae and land plant origins. Trends Ecol Evol. 2004, 19: 661-666. 10.1016/j.tree.2004.09.013.PubMedView ArticleGoogle Scholar
- Graham LE, Cook ME, Busse JS: The origin of plants: Body plan changes contributing to a major evolutionary radiation. PNAS. 2000, 97: 4535-4540. 10.1073/pnas.97.9.4535.PubMedPubMed CentralView ArticleGoogle Scholar
- Quinn GP, Keough MJ: Experimental design and data analysis for biologists. 2002, Cambridge: Cambridge University PressView ArticleGoogle Scholar
- Ohlrogge J, Benning C: Unraveling plant metabolism by EST analysis. Curr Opin Plant Biol. 2000, 3: 224-228.PubMedView ArticleGoogle Scholar
- Cerff R, Chambers SE: Subunit Structure of Higher-Plant Glyceraldehyde-3-Phosphate Dehydrogenases (Ec 18.104.22.168 and Ec 22.214.171.124). J Biol Chem. 1979, 254: 6094-6098.PubMedGoogle Scholar
- Becker B, Becker D, Kamerling JP, Melkonian M: 2-keto-sugar acids in green flagellates: A chemical marker for prasinophycean scales. JPhycol. 1991, 27: 498-504. 10.1111/j.0022-3646.1991.00498.x.Google Scholar
- Kanter U, Usadel B, Guerineau F, Li Y, Pauly M, Tenhaken R: The inositol oxygenase gene family of Arabidopsis is involved in the biosynthesis of nucleotide sugar precursors for cell-wall matrix polysaccharides. Planta. 2005, 221: 243-254. 10.1007/s00425-004-1441-0.PubMedView ArticleGoogle Scholar
- Delsuc F, Brinkmann H, Philippe H: Phylogenomics and the reconstruction of the tree of life. Nature Reviews Genetics. 2005, 6: 361-375. 10.1038/nrg1603.PubMedView ArticleGoogle Scholar
- Kimura M: The Neutral Theory of Molecular Evolution. 1983, Cambridge: Cambridge University PressView ArticleGoogle Scholar
- Fink RC, Scandalios JG: Molecular evolution and structure-function relationships of the superoxide dismutase gene families in angiosperms and their relationship to other eukaryotic and prokaryotic superoxide dismutases. Arch Biochem Biophys. 2002, 399: 19-36. 10.1006/abbi.2001.2739.PubMedView ArticleGoogle Scholar
- Dejesus MD, Tabatabai F, Chapman DJ: Taxonomic Distribution of Copper-Zinc Superoxide-Dismutase in Green-Algae and Its Phylogenetic Importance. J Phycol. 1989, 25: 767-772. 10.1111/j.0022-3646.1989.00767.x.View ArticleGoogle Scholar
- Frederics E, Gruber PJ, Tolbert NE: Occurrence of Glycolate Dehydrogenase and Glycolate Oxidase in Green Plants – Evolutionary Survey. Plant Physiol. 1973, 52: 318-323.View ArticleGoogle Scholar
- Igamberdiev AU, Lea PJ: The role of peroxisomes in the integration of metabolism and evolutionary diversity of photosynthetic organisms. Phytochemistry. 2002, 60: 651-674. 10.1016/S0031-9422(02)00179-6.PubMedView ArticleGoogle Scholar
- Schwender J, Gemunden C, Lichtenthaler HK: Chlorophyta exclusively use the 1-deoxyxylulose 5-phosphate/2- C-methylerythritol 4-phosphate pathway for the biosynthesis of isoprenoids. Planta. 2001, 212: 416-423. 10.1007/s004250000409.PubMedView ArticleGoogle Scholar
- Noguchi M, Sawadas T, Akazawa T: ATP-regenerating system in the cilia of Paramecium caudatum. Journal of Experimental Biology. 2001, 204: 1063-1071.PubMedGoogle Scholar
- Pazour GJ, Agrin N, Leszyk J, Witman GB: Proteomic analysis of a eukaryotic cilium. J Cell Biol. 2005, 170: 103-113. 10.1083/jcb.200504008.PubMedPubMed CentralView ArticleGoogle Scholar
- Pasqualato S, Renault L, Cherfils J: Arf, Arl, Arp and Sar proteins: a family of GTP-binding proteins with a structural device for 'front-back' communication. EMBO Rep. 2002, 3: 1035-1041. 10.1093/embo-reports/kvf221.PubMedPubMed CentralView ArticleGoogle Scholar
- Roberts AW, Roberts E: Cellulose synthase (CesA) genes in algae and seedless plants. Cellulose. 2004, 11: 419-435. 10.1023/B:CELL.0000046418.01131.d3.View ArticleGoogle Scholar
- Stabenau H, Winkler U: Glycolate metabolism in green algae. Physiol Plant. 2005, 123: 235-245. 10.1111/j.1399-3054.2005.00442.x.View ArticleGoogle Scholar
- Falkowski PG, Katz ME, Knoll AH, Quigg A, Raven JA, Schofield O, Taylor FJR: The evolution of modern eukaryotic phytoplankton. Science. 2004, 305: 354-360. 10.1126/science.1095964.PubMedView ArticleGoogle Scholar
- Badger MR, Price GD: CO2 concentrating mechanisms in cyanobacteria: molecular components, their diversity and evolution. J Exp Bot. 2003, 54: 609-622. 10.1093/jxb/erg076.PubMedView ArticleGoogle Scholar
- Zhu YY, Machleder EM, Chenchik A, Li R, Siebert PD: Reverse transcriptase template switching: a SMART approach for full-length cDNA library construction. Biotechniques. 2001, 30: 892-897.PubMedGoogle Scholar
- Shagin DA, Rebrikov DV, Kozhemyako VB, Altshuler IM, Shcheglov AS, Zhulidov PA, Bogdanova EA, Staroverov DB, Rasskazov VA, Lukyanov S: A novel method for SNP detection using a new duplex-specific nuclease from crab hepatopancreas. Genome Res. 2002, 12: 1935-1942. 10.1101/gr.547002.PubMedPubMed CentralView ArticleGoogle Scholar
- Tatusov RL, Fedorova ND, Jackson JD, Jacobs AR, Kiryutin B, Koonin EV, Krylov DM, Mazumder R, Mekhedov SL, Nikolskaya AN, Rao BS, Smirnov S, Sverdlov AV, Vasudevan S, Wolf YI, Yin JJ, Natale DA: The COG database: an updated version includes eukaryotes. Bmc Bioinformatics. 2003, 4: 41-10.1186/1471-2105-4-41.PubMedPubMed CentralView ArticleGoogle Scholar
- Tatusov RL, Galperin MY, Natale DA, Koonin EV: The COG database: a tool for genome-scale analysis of protein functions and evolution. Nucleic Acids Res. 2000, 28: 33-36. 10.1093/nar/28.1.33.PubMedPubMed CentralView ArticleGoogle Scholar
- Apweiler R, Attwood TK, Bairoch A, Bateman A, Birney E, Biswas M, Bucher P, Cerutti T, Corpet F, Croning MDR, Durbin R, Falquet L, Fleischmann W, Gouzy J, Hermjakob H, Hulo N, Jonassen I, Kahn D, Kanapin A, Karavidopoulou Y, Lopez R, Marx B, Mulder NJ, Oinn TM, Pagni M, Servant F, Sigrist CJ, Zdobnov EM: The InterPro database, an integrated documentation resource for protein families, domains and functional sites. Nucleic Acids Res. 2001, 29: 37-40. 10.1093/nar/29.1.37.PubMedPubMed CentralView ArticleGoogle Scholar
- Ruelland E, Miginiac-Maslow M: Regulation of chloroplast enzyme activities by thioredoxins: activation or relief from inhibition?. Trends Plant Sci. 1999, 4: 136-141. 10.1016/S1360-1385(99)01391-6.PubMedView ArticleGoogle Scholar
- Ocheretina O, Haferkamp I, Tellioglu H, Scheibe R: Light-modulated NADP-malate dehydrogenases from mossfern and green algae: insights into evolution of the enzyme's regulation. Gene. 2000, 258: 147-154. 10.1016/S0378-1119(00)00409-1.PubMedView ArticleGoogle Scholar
- Lemaire SD, Quesada A, Merchan F, Corral JM, Igeno MI, Keryer E, Issakidis-Bourguet E, Hirasawa M, Knaff DB, Miginiac-Maslow M: NADP-malate dehydrogenase from unicellular green alga Chlamydomonas reinhardtii. A first step toward redox regulation. Plant Physiol. 2005, 137: 514-521. 10.1104/pp.104.052670.PubMedPubMed CentralView ArticleGoogle Scholar
- Portis AR: Rubisco activase – Rubisco's catalytic chaperone. Photosynth Res. 2003, 75: 11-27. 10.1023/A:1022458108678.PubMedView ArticleGoogle Scholar
- Schurmann P, Jacquot JP: Plant thioredoxin systems revisited. Annu Rev Plant Physiol Plant Molec Biol. 2000, 51: 371-400. 10.1146/annurev.arplant.51.1.371.View ArticleGoogle Scholar
This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.