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c-type cytochromes are characterized by the presence of two covalent bonds linking heme to apocytochrome and by the heme attachment motif in the apoprotein. Several molecular systems for the maturation of c-type cytochromes have evolved in different organisms. The best characterized are three of them: system I, system II and system III. Heme is synthesized in bacterial cytoplasm, in plastids, and in animal and fungal mitochondria. Therefore the maturation of bacterial and plastid c-type cytochromes involves the transport of heme and apocytochrome from the n-side to the p-side of the respective biological membranes and the formation of the covalent bond at the p-side. It should be underlined that the site of the c-type apocytochrome synthesis is also distinct from the site of its functioning. The aim of this review is to present the current state of knowledge concerning the structure and function of two systems – system I and system II – in the maturation of plant mitochondrial and plastid c-type cytochromes, respectively.
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The Glaucophyta: the blue-green plants in a nutshell

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The Glaucophyta is one of the three major lineages of photosynthetic eukaryotes, together with viridiplants and red algae, united in the presumed monophyletic supergroup Archaeplastida. Glaucophytes constitute a key algal lineage to investigate both the origin of primary plastids and the evolution of algae and plants. Glaucophyte plastids possess exceptional characteristics retained from their cyanobacterial ancestor: phycobilisome antennas, a vestigial peptidoglycan wall, and carboxysome-like bodies. These latter two traits are unique among the Archaeplastida and have been suggested as evidence that the glaucophytes diverged earliest during the diversification of this supergroup. Our knowledge of glaucophytes is limited compared to viridiplants and red algae, and this has restricted our capacity to untangle the early evolution of the Archaeplastida. However, in recent years novel genomic and functional data are increasing our understanding of glaucophyte biology. Diverse comparative studies using information from the nuclear genome of Cyanophora paradoxa and recent transcriptomic data from other glaucophyte species provide support for the common origin of Archaeplastida. Molecular and ultrastructural studies have revealed previously unrecognized diversity in the genera Cyanophora and Glaucocystis. Overall, a series of recent findings are modifying our perspective of glaucophyte diversity and providing fresh approaches to investigate the basic biology of this rare algal group in detail.
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Stromuling when stressed!

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Stromules are stroma-filled tubules, extruding from the plastid and surrounded by both envelope membranes, but so far, stromules remain enigmatic structures and their function unknown. Stromules can interconnect plastids and have been found to associate with the nucleus, endoplasmic reticulum, Golgi complex, plasma membrane, mitochondria and peroxisomes. This minireview briefly summarizes markers to visualize stromules, inducers of stromules and provides new data about plant virus induced stromules.
A single origin of plastids and the monophyly of three “primary” plastid-containing groups – the Chloroplastida (or Viridiplantae; green algae+land plants), Rhodophyta, and Glaucophyta – are widely accepted, mainstream hypotheses that form the basis for many comparative evolutionary studies. This “Archaeplastida” hypothesis, however, thus far has not been unambiguously confirmed by phylogenetic studies based on nucleocytoplasmic markers. In view of this as well as other lines of evidence, we suggest the testing of an alternate hypothesis that plastids of the Chloroplastida are of secondary origin. The new hypothesis is in agreement with, or perhaps better explains, existing data, including both the plastidal and nucleocytoplasmic characteristics of the Chloroplastida in comparison to those of other groups.
This review focuses on plant-to-plant horizontal gene transfer (HGT) involving the three DNA-containing cellular compartments. It highlights the great incidence of HGT in the mitochondrial genome (mtDNA) of angiosperms, the increasing number of examples in plant nuclear genomes, and the lack of any convincing evidence for HGT in the well-studied plastid genome of land plants. Most of the foreign mitochondrial genes are non-functional, generally found as pseudogenes in the recipient plant mtDNA that maintains its functional native genes. The few exceptions involve chimeric HGT, in which foreign and native copies recombine leading to a functional and single copy of the gene. Maintenance of foreign genes in plant mitochondria is probably the result of genetic drift, but a possible evolutionary advantage may be conferred through the generation of genetic diversity by gene conversion between native and foreign copies. Conversely, a few cases of nuclear HGT in plants involve functional transfers of novel genes that resulted in adaptive evolution. Direct cell-to-cell contact between plants (e.g. host-parasite relationships or natural grafting) facilitate the exchange of genetic material, in which HGT has been reported for both nuclear and mitochondrial genomes, and in the form of genomic DNA, instead of RNA. A thorough review of the literature indicates that HGT in mitochondrial and nuclear genomes of angiosperms is much more frequent than previously expected and that the evolutionary impact and mechanisms underlying plant-to-plant HGT remain to be uncovered.
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A sea slug’s guide to plastid symbiosis

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Some 140 years ago sea slugs that contained chlorophyll-pigmented granules similar to those of plants were described. While we now understand that these “green granules” are plastids the slugs sequester from siphonaceous algae upon which they feed, surprisingly little is really known about the molecular details that underlie this one of a kind animal-plastid symbiosis. Kleptoplasts are stored in the cytosol of epithelial cells that form the slug’s digestive tubules, and one would guess that the stolen organelles are acquired for their ability to fix carbon, but studies have never really been able to prove that. We also do not know how the organelles are distinguished from the remaining food particles the slugs incorporate with their meal and that include algal mitochondria and nuclei. We know that the ability to store kleptoplasts long-term has evolved only a few times independently among hundreds of sacoglossan species, but we have no idea on what basis. Here we take a closer look at the history of sacoglossan research and discuss recent developments. We argue that, in order to understand what makes this symbiosis work, we will need to focus on the animal’s physiology just as much as we need to commence a detailed analysis of the plastids’ photobiology. Understanding kleptoplasty in sacoglossan slugs requires an unbiased multidisciplinary approach.
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Plastid origin: who, when and why?

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The origin of plastids is best explained by endosymbiotic theory, which dates back to the early 1900s. Three lines of evidence based on protein import machineries and molecular phylogenies of eukaryote (host) and cyanobacterial (endosymbiont) genes point to a single origin of primary plastids, a unique and important event that successfully transferred two photosystems and oxygenic photosynthesis from prokaryotes to eukaryotes. The nature of the cyanobacterial lineage from which plastids originated has been a topic of investigation. Recent studies have focused on the branching position of the plastid lineage in the phylogeny based on cyanobacterial core genes, that is, genes shared by all cyanobacteria and plastids. These studies have delivered conflicting results, however. In addition, the core genes represent only a very small portion of cyanobacterial genomes and may not be a good proxy for the rest of the ancestral plastid genome. Information in plant nuclear genomes, where most genes that entered the eukaryotic lineage through acquisition from the plastid ancestor reside, suggests that heterocyst-forming cyanobacteria in Stanier’s sections IV and V are most similar to the plastid ancestor in terms of gene complement and sequence conservation, which is in agreement with models suggesting an important role of nitrogen fixation in symbioses involving cyanobacteria. Plastid origin is an ancient event that involved a prokaryotic symbiont and a eukaryotic host, organisms with different histories and genome evolutionary processes. The different modes of genome evolution in prokaryotes and eukaryotes bear upon our interpretations of plastid phylogeny.
The rhizarian amoeba Paulinella chromatophora harbors two photosynthetic cyanobacterial endosymbionts (chromatophores), acquired independently of primary plastids of glaucophytes, red algae and green plants. These endosymbionts have lost many essential genes, and transferred substantial number of genes to the host nuclear genome via endosymbiotic gene transfer (EGT), including those involved in photosynthesis. This indicates that, similar to primary plastids, Paulinella endosymbionts must have evolved a transport system to import their EGT-derived proteins. This system involves vesicular trafficking to the outer chromatophore membrane and presumably a simplified Tic-like complex at the inner chromatophore membrane. Since both sequenced Paulinella strains have been shown to undergo differential plastid gene losses, they do not have to possess the same set of Toc and Tic homologs. We searched the genome of Paulinella FK01 strain for potential Toc and Tic homologs, and compared the results with the data obtained for Paulinella CCAC 0185 strain, and 72 cyanobacteria, eight Archaeplastida as well as some other bacteria. Our studies revealed that chromatophore genomes from both Paulinella strains encode the same set of translocons that could potentially create a simplified but fully-functional Tic-like complex at the inner chromatophore membranes. The common maintenance of the same set of translocon proteins in two Paulinella strains suggests a similar import mechanism and/or supports the proposed model of protein import. Moreover, we have discovered a new putative Tic component, Tic62, a redox sensor protein not identified in previous comparative studies of Paulinella translocons.
Eukaryotes co-opted photosynthetic carbon fixation from prokaryotes by engulfing a cyanobacterium and stably integrating it as a photosynthetic organelle (plastid) in a process known as primary endosymbiosis. The sheer complexity of interactions between a plastid and the surrounding cell that started to evolve over 1 billion years ago, make it challenging to reconstruct intermediate steps in organelle evolution by studying extant plastids. Recently, the photosynthetic amoeba Paulinella chromatophora was identified as a much sought-after intermediate stage in the evolution of a photosynthetic organelle. This article reviews the current knowledge on this unique organism. In particular it describes how the interplay of reductive genome evolution, gene transfers, and trafficking of host-encoded proteins into the cyanobacterial endosymbiont contributed to transform the symbiont into a nascent photosynthetic organelle. Together with recent results from various other endosymbiotic associations a picture emerges that lets the targeting of host-encoded proteins into bacterial endosymbionts appear as an early step in the establishment of an endosymbiotic relationship that enables the host to gain control over the endosymbiont.
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