Figure 1 illustrates the various endosymbiotic events described here. Amongst eukaryotes, the apicomplexan parasitic pathogens Toxoplasma and Plasmodium have curious cytoplasmic organelles bounded by three membranes, namely 'apicoplasts', which genome sequencing has established as bona fide plastids complete with a characteristic inverted repeat within the plastid genome [ 9 ]. The presence of three membranes, as is found around chloroplasts of dinoflagellates and euglenoids, betrays an ancestry from a secondary symbiosis, as does the presence of four membranes surrounding the plastids of, for example, photosynthetic heterokonts a diverse group, some of which are algae such as diatoms and brown algae.
The function of the apicoplast is not clearly understood, but one suggestion is that it is indispensable for the synthesis of iron-sulfur proteins.
The function of the residual plastid genome is even less clear, and it provides a test case for any theory for the function of organellar genes. Although Plasmodium has a plastid genome that some think is on the way out, trypanosomes, which are also non-photosynthetic, have no plastid or plastid genome at all, but are now clearly seen to be former euglenoids because of the remaining genes for a variety of plant-like enzymes, including sedoheptulose-1,7-bisphosphatase otherwise found only in the Benson-Calvin cycle [ 10 , 11 ].
The article by Martin et al. An important conclusion from this analysis is that two secondary endosymbiotic events involving a red alga are needed to explain the occurrence of plastids in cryptophytes algae with phycobilin pigments in the thylakoid lumen rather than in particles on the thylakoid membrane as in cyanobacterial and red algae; an example is Guillardia and heterokonts the diatom Odontella.
This contrasts with the arguments of Cavalier-Smith recently set out in [ 12 ] for a single endosymbiotic event, based on evidence such as the replacement of the glyceraldehydephosphate dehydrogenase gene derived from the red algal plastid with one of host origin in both cases.
Another recent article [ 13 ] deals with genome-based phylogenies of plastids; 19 complete chloroplast genomes are studied using a new computational method, and broadly similar conclusions are reached to those of Martin and co-workers [ 6 ]. This work also allows novel functional assignments to a number of chloroplast open reading frames. The functional implications of chloroplast genomics, with special reference to experimental opportunities and 'directional genetics' in Arabidopsis thaliana , have recently been reviewed by Leister [ 14 ].
An important question relating to the evolution of plastid genomes in higher plants is the timing of the changes in the plastid genome in the streptophyte clade made up of charophytes, a group of green algae or chlorophytes, plus embryophytes, or higher plants , which evolved more than million years ago.
From the unicellular flagellate Mesostigma , which is either a basal chlorophyte or lies at the split between Chlorophyta and Streptophyta, to the embryophytes, of which the liverwort Marchantia is the most basal to have been sequenced, the changes are gene losses, including transfer to the nucleus, scrambling of gene order, and intron insertion [ 15 ].
An important contribution to bridging the evolutionary gap between Mesostigma and Marchantia is the work of Turmel et al. Before the work of Turmel et al. The complete plastid genome sequence of Chaetosphaeridium globosum [ 15 ] shows that most of the embryophyte characteristics were present in the charophyte alga, so that the major changes had occurred between the branch to Mesostigma and that to Chaetosphaeridium.
The common features shared by the plastid DNA of Chaetosphaeridium and of embryophytes include the gene content, the intron composition, and the gene order. Thus, the Chaetosphaeridium chloroplast genome has genes compared to in Mesostigma and in embryophytes , one Group I intron there are none in Mesostigma and one in embryophytes , 16 cis -spliced Group II introns none in Mesostigma and in embryophytes and one trans -spliced Group II intron none in Mesostigma , one in embryophytes.
Genome size kilobases is relatively constant among Mesostigma, Chaetosphaeridium and higher plant plastids. By contrast, the mitochondrial genome of Chaetosphaeridium is closely similar to that of Mesostigma in terms of size 57 kb and 42 kb, respectively , gene content and, perhaps, intron content. Chaetosphaeridium has a much smaller genome size than the obese mitochondrial genomes of Marchantia kb or Arabidopsis kb , and many more cis -spliced Group II introns rather than two.
The apparently different tempo of evolution in mitochondria and plastids of the charophytes deserves further investigation. An important point about the functional genomics of the plastid is the determinant of which genes essential for plastid function are retained in the plastid genome. Higher plant plastid genomes have slightly fewer genes than in the plastids of the charophytes sensu lato that is, the charophytes sensu stricto plus Mesostigma.
One requirement of the endosymbiont hypothesis is whole-scale gene transfer from the chloroplast to the nucleus. Long thought to be either impossible or, at best, highly problematical, its difficulties are often thought to relate to the failure of some genes to move at all.
Gene transfer from chloroplast to nucleus is now estimated to occur naturally in tobacco at a frequency of one transposition in 16, pollen grains [ 16 ]. In natural populations and over evolutionary time, this frequency represents a massive informational onslaught and highlights the urgency of the question of why chloroplasts have genomes at all.
There must be some crucial, over-riding, selective advantage in retaining certain genes in chloroplasts but not others. Evidence is now accruing for the ten-year-old proposal that gene expression in the chloroplast is regulated by the function of a core of chloroplast gene products in photosynthesis and electron transport [ 17 , 18 ].
It is clear that genomics, in the sense of whole-genome analyses, is making very important contributions to our understanding of the evolution of plastids, and is complementing, and to a significant extent supplanting, 'single gene' phylogenies.
Genomics is revolutionizing our understanding of the changes involved in the primary endosymbiosis that produced the plastids of red, green and glaucophyte algae, and in the subsequent genetic changes in green charophycean plastids with the evolution of higher plants.
Genomics is also indispensable for understanding how red and green algae yielded the plastids derived from secondary endosymbiosis. The endosymbiont hypothesis took a long time to graduate from wild and untestable speculation to an accepted view of plastid origins and evolution.
In contrast, comparative genomics has quickly elevated the kinship of chloroplasts and cyanobacteria to a keystone of our understanding of the most abundant of cells, the primary producers on which life now depends, not to mention some vicious and enterprising pathogens whose exploits are a global burden to human health. The title of this article asks what the cyanobacteria have done for plants. Biol Centralbl.
Google Scholar. Eur J Phycol. Margulis L: Symbiosis in Cell Evolution. The Arabidopsis Genome Initiative: Analysis of the genome sequence of the flowering plant Arabidopsis thaliana.
Article Google Scholar. Genome Res. Martin W, Borst P: Secondary loss of chloroplasts in trypanosomes. Algae represent an ancient group of plant like organisms, comprising a heterogeneous, polyphyletic assemblage of prokaryotes and eukaryotes, which have been primarily classified on the basis of their pigments, storage food material and cell wall characteristics.
DNA evidence suggests that the first eukaryotes green plants evolved from prokaryotes through endosymbiotic events between and million years ago. Among algae, blue green algae or cyanobacteria represent an ancient group of photosynthetic prokaryotes, whose ubiquity, metabolic flexibility and adaptive abilities have made them a subject of research worldwide.
Their biological significance, especially as the prokaryotic interface between the primeval photosynthetic cell and present day plants is also well recognized. However, in the current scenario, with the advent of molecular phylogenetics and the expanding knowledge regarding the evolution of life through the use of bioinformatics, a thorough re-evaluation of algae and interrelationships with plants is needed.
This compilation attempts to link Darwinism, Neo-Darwinism and Systemic Darwinism, with the rapidly generated information through modern molecular tools for a better understanding of evolution of land plants, as mediated through algae and endosymbiotic events combined with horizontal and lateral gene transfer processes.
Unable to display preview. Download preview PDF. Skip to main content. This service is more advanced with JavaScript available. Advertisement Hide. Evolutionary relationships among cyanobacteria, algae and plants: Revisited in the light of Darwinism.
Not surprisingly, RuBisCO is widely conserved across species, but some of its natural variants are slightly more effective than others. For instance, heterologous expression of RuBisCO from the purple-sulfur bacterium Allochromatium vinosum in Synechococcus elongatus sp. Therefore, metagenomic analysis of natural RuBisCO diversity may identify superior enzymes to be engineered into a cyanobacterial host for detailed characterization and platform improvement.
In some cyanobacteria, the rbcX gene co-localizes with the genes encoding RbcL and RbcS in the chromosome. This enzyme is widely distributed in all plants and many bacteria. Attempts to improve plant CO 2 fixation by expression of a cyanobacterial PEPC with diminished sensitivity to feedback inhibition have been unsuccessful; the resulting transgenic plants even showed decreased fitness Chen et al.
In the cytosol of cyanobacteria, RuBisCO is found in proteinaceous microcompartments known as carboxysomes Kerfeld et al. A carboxysome consists of a shell assembled from roughly protein hexamers, forming the 20 facets of an icosahedron, and 12 pentamers that form its corners Heinhorst et al. The carboxysome encapsulates RuBisCO complexes and plays a central role in a mechanism that concentrates inorganic carbon providing enough CO 2 for the enzyme to favor the carboxylase reaction.
The number of carboxysomes and the expression levels of carboxysome genes increase significantly when cyanobacterial cells are limited for CO 2 Heinhorst et al. Carboxysomes can potentially be exploited as synthetic compartments, similar to eukaryotic organelles, to rationally organize pathways or networks within a spatially distinct subsystem Kerfeld et al. If photosynthetic organisms are to be used as a platform for pathways devoted to the biosynthesis of terpenoid- or fatty acid-derived products, this product-to-biomass carbon portioning must be increased significantly.
The aim of synthetic biology is to engineer biological systems by designing and constructing novel modules to perform new functions for useful purposes. In this context, the photosynthetic complexes PS I and II in the thylakoids of cyanobacteria can be regarded as building blocks, which can be integrated into novel biosynthetic pathways.
Ideally, the biosynthetic pathway should be located in the thylakoids or at least in close proximity to the photosynthetic electron transfer chain, allowing the biosynthetic enzymes to tap directly into photosynthetic electron transport and energy generation, and even draw on carbon skeletons derived from CO 2 fixation.
Recently, an entire cytochrome Pdependent pathway has been relocated to the thylakoids of tobacco chloroplasts and shown to be driven directly by the reducing power generated by photosynthesis in a light-dependent manner Zygadlo Nielsen et al.
This demonstrates the potential of transferring pathways for structurally complex chemicals to the chloroplast and using photosynthesis to drive the Ps with water as the primary electron donor. Synthetic biology in cyanobacteria still lags behind conventional species such as E. Some progress has been made in redirecting photosynthetically fixed carbon toward commercially interesting compounds. The C 5 molecule isoprene is a volatile hydrocarbon that can be used as fuel and as a platform-chemical for production of synthetic rubber and high-value compounds.
For photosynthetic generation of isoprene in cyanobacteria, the isoprene synthase gene from the plant Pueraria montana kudzu has been successfully expressed in Synechocystis and isoprene was indeed produced Lindberg et al.
However, drastic metabolic engineering will be required to redirect carbon partitioning away from the dominant carbohydrate biosynthesis toward terpenoid biosynthesis. In fact, heterologous expression of the isoprene synthase in combination with the introduction of a non-native mevalonic acid pathway for increased carbon flux toward isopentenyl-diphosphate IPP and dimethylallyl-diphosphate DMAPP precursors of isoprene resulted in a 2.
Tightly regulated and inducible protein expression is an important prerequisite for product yield and predictability in synthetic biology approaches. In this context, riboswitches are attracting increasing interest. Riboswitches are functional non-coding RNA molecules that play a crucial role in gene regulation at the transcriptional or post-transcriptional level in many bacteria Roth and Breaker, In general, the sensing domain aptamer of riboswitches is combined with a regulating domain.
The regulating domain can comprise several types of expression platforms to control gene expression.
For instance, direct binding of a specific ligand to the aptamer domain can be used to attenuate transcription termination or translation initiation Roth and Breaker, Recently, a theophylline-dependent riboswitch was established as a strict and inducible protein expression system in S. In the ON state, protein expression levels were up to fold higher than in the absence of the activator.
Moreover, it was possible to fine-tune the level of protein expression by using a defined range of theophylline concentrations. Cyanobacteria are receiving increasing interest as experimental scaffolds for the modification of their endogenous photosynthetic machineries, as well as the integration and engineering of modules of plant photosynthesis. Therefore, we believe that cyanobacteria will be extensively used by many plant biologists as additional model system in future analyses.
Indeed, for the identification of the entire set of components necessary for photosynthesis only cyanobacteria are suitable as experimental platforms. If this is achieved, the next goal is to transfer this photosynthetic module to other non-photosynthetic organisms like E.
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. Andersson, I. Structure and function of Rubisco. Plant Physiol. CrossRef Full Text. Beckmann, J. Improvement of light to biomass conversion by de-regulation of light-harvesting protein translation in Chlamydomonas reinhardtii.
Bentley, F. Heterologous expression of the mevalonic acid pathway in cyanobacteria enhances endogenous carbon partitioning to isoprene. Plant 7, 71— Chen, L.
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