Synonymous Codon Usage Bias in the Plastid Genome is Unrelated to Gene Structure and Shows Evolutionary Heterogeneity.
ABSTRACT: Synonymous codon usage bias (SCUB) is the nonuniform usage of codons, occurring often in nearly all organisms. Our previous study found that SCUB is correlated with intron number, is unequal among exons in the plant nuclear genome, and mirrors evolutionary specialization. However, whether this rule exists in the plastid genome has not been addressed. Here, we present an analysis of SCUB in the plastid genomes of 25 species from lower to higher plants (algae, bryophytes, pteridophytes, gymnosperms, and spermatophytes). We found NNA and NNT (A- and T-ending codons) are preferential in the plastid genomes of all plants. Interestingly, this preference is heterogeneous among taxonomies of plants, with the strongest preference in bryophytes and the weakest in pteridophytes, suggesting an association between SCUB and plant evolution. In addition, SCUB frequencies are consistent among genes with varied introns and among exons, indicating that the bias of NNA and NNT is unrelated to either intron number or exon position. Further, SCUB is associated with DNA methylation-induced conversion of cytosine to thymine in the vascular plants but not in algae or bryophytes. These data demonstrate that these SCUB profiles in the plastid genome are distinctly different compared with the nuclear genome.
Project description:Synonymous codon usage bias (SCUB) is a common event that a non-uniform usage of codons often occurs in nearly all organisms. We previously found that SCUB is correlated with both intron number and exon position in the plant nuclear genome but not in the plastid genome; SCUB in both nuclear and plastid genome can mirror the evolutionary specialization. However, how about the rules in the mitochondrial genome has not been addressed. Here, we present an analysis of SCUB in the mitochondrial genome, based on 24 plant species ranging from algae to land plants. The frequencies of NNA and NNT (A- and T-ending codons) are higher than those of NNG and NNC, with the strongest preference in bryophytes and the weakest in land plants, suggesting an association between SCUB and plant evolution. The preference for NNA and NNT is more evident in genes harboring a greater number of introns in land plants, but the bias to NNA and NNT exhibits even among exons. The pattern of SCUB in the mitochondrial genome differs in some respects to that present in both the nuclear and plastid genomes.
Project description:Synonymous codon usage bias (SCUB) of both nuclear and organellar genes can mirror the evolutionary specialization of plants. The polyploidization process exposes the nucleus to genomic shock, a syndrome which promotes, among other genetic variants, SCUB. Its effect on organellar genes has not, however, been widely addressed. The present analysis targeted the chloroplast genomes of two leading polyploid crop species, namely cotton and bread wheat. The frequency of codons in the chloroplast genomes ending in either adenosine (NNA) or thymine (NNT) proved to be higher than those ending in either guanidine or cytosine (NNG or NNC), and this difference was conserved when comparisons were made between polyploid and diploid forms in both the cotton and wheat taxa. Preference for NNA/T codons was heterogeneous among genes with various numbers of introns and was also differential among the exons. SCUB patterns distinguished tetraploid cotton from its diploid progenitor species, as well as bread wheat from its diploid/tetraploid progenitor species, indicating that SCUB in the chloroplast genome partially mirrors the formation of polyploidies.
Project description:<h4>Background</h4>Evidence has been assembled to suggest synonymous codon usage bias (SCUB) has close relationship with intron. However, the relationship (if any) between SCUB and intron number as well as exon position is at present rather unclear.<h4>Results</h4>To explore this relationship, the sequences of a set of genes containing between zero and nine introns was extracted from the published genome sequences of three algal species, one moss, one fern and six angiosperms (three monocotyledonous species and three dicotyledonous species). In the algal genomes, the frequency of synonymous codons of the form NNG/NNC (codons with G and C at the third position) was positively related to intron number, but that of NNA/NNT was inversely correlated; the opposite was the case in the land plant genomes. The frequency of NNC/NNG was higher and that of NNA/NNT lower in two terminal exons than in the interstitial exons in the land plant genes, but the rule showed to be opposite in the algal genes. SCUB patterns in the interstitial and two terminal exons mirror the different evolutionary relationships between these plant species, while the first exon shows the highest level of conservation is therefore concluded to be the one which experiences the heaviest selection pressure. The phenomenon of SCUB may also be related to DNA methylation induced conversion of CG to AT.<h4>Conclusions</h4>These data provide some evidence of linkage between SCUB, the evolution of introns and DNA methylation, which brings about a new perspective for understanding how genomic variation is created during plant evolution.
Project description:Chloroplasts are unique organelles within the plant cells and are responsible for sustaining life forms on the earth due to their ability to conduct photosynthesis. Multiple functional genes within the chloroplast are responsible for a variety of metabolic processes that occur in the chloroplast. Considering its fundamental role in sustaining life on the earth, it is important to identify the level of diversity present in the chloroplast genome, what genes and genomic content have been lost, what genes have been transferred to the nuclear genome, duplication events, and the overall origin and evolution of the chloroplast genome. Our analysis of 2511 chloroplast genomes indicated that the genome size and number of coding DNA sequences (CDS) in the chloroplasts genome of algae are higher relative to other lineages. Approximately 10.31% of the examined species have lost the inverted repeats (IR) in the chloroplast genome that span across all the lineages. Genome-wide analyses revealed the loss of the Rbcl gene in parasitic and heterotrophic plants occurred approximately 56 Ma ago. PsaM, Psb30, ChlB, ChlL, ChlN, and Rpl21 were found to be characteristic signature genes of the chloroplast genome of algae, bryophytes, pteridophytes, and gymnosperms; however, none of these genes were found in the angiosperm or magnoliid lineage which appeared to have lost them approximately 203-156 Ma ago. A variety of chloroplast-encoded genes were lost across different species lineages throughout the evolutionary process. The Rpl20 gene, however, was found to be the most stable and intact gene in the chloroplast genome and was not lost in any of the analyzed species, suggesting that it is a signature gene of the plastome. Our evolutionary analysis indicated that chloroplast genomes evolved from multiple common ancestors ~1293 Ma ago and have undergone vivid recombination events across different taxonomic lineages.
Project description:It is generally believed that bryophytes are the earliest land plants. However, the phylogenetic relationships among bryophytes, including mosses, liverworts and hornworts, are not clearly resolved. To obtain more information on the earliest land plants, we determined the complete nucleotide sequence of the chloroplast genome from the hornwort Anthoceros formosae. The circular double-stranded DNA of 161 162 bp is the largest genome ever reported among land plant chloroplasts. It contains 76 protein, 32 tRNA and 4 rRNA genes and 10 open reading frames (ORFs), which are identical with the chloroplast genome of the other green plants analyzed. The major difference is a larger inverted repeat than that of the liverwort Marchantia, Anthoceros contains an excess of ndhB and rps7 genes and the 3' exon of rps12. The genes matK and rps15, commonly found in the chloroplast genomes of land plants, are pseudogenes. The intron of rrn23 is the first finding in the known chloroplast genomes of land plants. A striking feature of the hornwort chloroplast is that more than half of the protein-coding genes have nonsense codons, which are converted into sense codons by RNA editing. Maximum-likelihood (ML) analysis, based on 11 518 amino acid sites of 52 proteins encoded in the chloroplast genomes of the green plants, placed liverworts as the sister to all other land plants.
Project description:The forfeiting of photosynthetic capabilities has occurred independently many times throughout eukaryotic evolution. But almost all non-photosynthetic plants and algae still retain a colorless plastid and an associated genome, which performs fundamental processes apart from photosynthesis. Unfortunately, little is known about the forces leading to photosynthetic loss; this is largely because there is a lack of data from transitional species. Here, we compare the plastid genomes of two "transitional" green algae: the photosynthetic, mixotrophic Auxenochlorella protothecoides and the non-photosynthetic, obligate heterotroph Prototheca wickerhamii. Remarkably, the plastid genome of A. protothecoides is only slightly larger than that of P. wickerhamii, making it among the smallest plastid genomes yet observed from photosynthetic green algae. Even more surprising, both algae have almost identical plastid genomic architectures and gene compositions (with the exception of genes involved in photosynthesis), implying that they are closely related. This close relationship was further supported by phylogenetic and substitution rate analyses, which suggest that the lineages giving rise to A. protothecoides and P. wickerhamii diverged from one another around six million years ago.
Project description:When the sequence of the Euglena gracilis chloroplast genome was reported in 1993 the alpha-subunit gene (rpoA) of RNA polymerase appeared to be missing, based on a comparison of all putative reading frames to the then known rpoA loci. Since there has been a large increase in known rpoA sequences, the question of a Euglena chloroplast rpoA gene was re-examined. A previously described unknown reading frame of 161 codons was found to be part of an rpoA gene split by a single group III intron. This rpoA gene, which is highly variable from species to species, was then isolated and characterized in five other euglenoid species, Euglena anabaena, Euglena granulata, Euglena myxocylindracea, Euglena stellata and Euglena viridis, and in the Astasia longa plastid genome. All seven Euglena rpoA genes have either one or three group III introns. The rpoA gene products in Euglena spp. appear to be the most variable in this gene family when compared to the rpoA gene in other species of bacteria, algae and plants. Additionally, Euglena rpoA proteins lack a C-terminal domain required for interaction with some regulatory proteins, a feature shared only with some chlorophyte green algae. The E.gracilis rpoA gene is the distal cistron of a multigene cluster that includes genes for carbohydrate biosynthesis, photosynthetic electron transport, an antenna complex and ribosomal proteins. This study provides new insights into the transcription system of euglenoid plastids, the organization of the plastid genome, group III intron evolution and euglenoid phylogeny.
Project description:Since the endosymbiotic origin of chloroplasts from cyanobacteria 2 billion years ago, the evolution of plastids has been characterized by massive loss of genes. Most plants and algae depend on photosynthesis for energy and have retained ?110 genes in their chloroplast genome that encode components of the gene expression machinery and subunits of the photosystems. However, nonphotosynthetic parasitic plants have retained a reduced plastid genome, showing that plastids have other essential functions besides photosynthesis. We sequenced the complete plastid genome of the underground orchid, Rhizanthella gardneri. This remarkable parasitic subterranean orchid possesses the smallest organelle genome yet described in land plants. With only 20 proteins, 4 rRNAs, and 9 tRNAs encoded in 59,190 bp, it is the least gene-rich plastid genome known to date apart from the fragmented plastid genome of some dinoflagellates. Despite numerous differences, striking similarities with plastid genomes from unrelated parasitic plants identify a minimal set of protein-encoding and tRNA genes required to reside in plant plastids. This prime example of convergent evolution implies shared selective constraints on gene loss or transfer.
Project description:It has been known that PSI and PSII supercomplexes are involved in the linear and cyclic electron transfer, dynamics of light capture, and the repair cycle of PSII under environmental stresses. However, evolutions of photosystem (PS) complexes from evolutionarily divergent species are largely unknown. Here, we improved the blue native polyacrylamide gel electrophoresis (BN-PAGE) separation method and successfully separated PS complexes from all terrestrial plants. It is well known that reversible D1 protein phosphorylation is an important protective mechanism against oxidative damages to chloroplasts through the PSII photoinhibition-repair cycle. The results indicate that antibody-detectable phosphorylation of D1 protein is the latest event in the evolution of PS protein phosphorylation and occurs exclusively in seed plants. Compared to angiosperms, other terrestrial plant species presented much lower contents of PS supercomplexes. The amount of light-harvesting complexes II (LHCII) trimers was higher than that of LHCII monomers in angiosperms, whereas it was opposite in gymnosperms, pteridophytes, and bryophytes. LHCII assembly may be one of the evolutionary characteristics of vascular plants. <i>In vivo</i> chloroplast fluorescence measurements indicated that lower plants (bryophytes especially) showed slower changes in state transition and nonphotochemical quenching (NPQ) in response to light shifts. Therefore, the evolution of PS supercomplexes may be correlated with their acclimations to environments.
Project description:BACKGROUND AND AIMS: In angiosperms xyloglucan endotransglucosylase (XET)/hydrolase (XTH) is involved in reorganization of the cell wall during growth and development. The location of oligo-xyloglucan transglucosylation activity and the presence of XTH expressed sequence tags (ESTs) in the earliest diverging extant plants, i.e. in bryophytes and algae, down to the Phaeophyta was examined. The results provide information on the presence of an XET growth mechanism in bryophytes and algae and contribute to the understanding of the evolution of cell wall elongation in general. METHODS: Representatives of the different plant lineages were pressed onto an XET test paper and assayed. XET or XET-related activity was visualized as the incorporation of fluorescent signal. The Physcomitrella genome database was screened for the presence of XTHs. In addition, using the 3' RACE technique searches were made for the presence of possible XTH ESTs in the Charophyta. KEY RESULTS: XET activity was found in the three major divisions of bryophytes at sites corresponding to growing regions. In the Physcomitrella genome two putative XTH-encoding cDNA sequences were identified that contain all domains crucial for XET activity. Furthermore, XET activity was located at the sites of growth in Chara (Charophyta) and Ulva (Chlorophyta) and a putative XTH ancestral enzyme in Chara was identified. No XET activity was identified in the Rhodophyta or Phaeophyta. CONCLUSIONS: XET activity was shown to be present in all major groups of green plants. These data suggest that an XET-related growth mechanism originated before the evolutionary divergence of the Chlorobionta and open new insights in the evolution of the mechanisms of primary cell wall expansion.