It has recently emerged that malarial, toxoplasmodial and related parasites contain a vestigial plastid (the organelle in which photosynthesis occurs in plants and algae). The function of the plastid in these obligate intracellular parasites has not been established. It seems likely that modern apicomplexans derive from photosynthetic predecessors, which perhaps formed associations with protists and invertebrates and abandoned autotrophy in favour of parasitism. Recognition of a third genetic compartment in these parasites proffers alternative strategies for combating a host of important (...) human and animal diseases. It also poses some fascinating questions about the evolutionary biology of this important group of pathogens. (shrink)

Some nuclear‐encoded proteins are imported into higher plant plastids via the endomembrane (EM) system. Compared with multi‐protein Toc and Tic translocons required for most plastid protein import, the relatively uncomplicated nature of EM trafficking led to suggestions that it was the original transport mechanism for nuclear‐encoded endosymbiont proteins, and critical for the early stages of plastid evolution. Its apparent simplicity disappears, however, when EM transport is considered in light of selective constraints likely encountered during the conversion of stable endosymbionts (...) into fully integrated organelles. From this perspective it is more parsimonious to presume the early evolution of post‐translational protein import via simpler, ancestral forms of modern Toc and Tic plastid translocons, with EM trafficking arising later to accommodate glycosylation and/or protein targeting to multiple cellular locations. This hypothesis is supported by both empirical and comparative data, and is consistent with the relative paucity of EM‐based transport to modern primary plastids. (shrink)

Retrograde plastid‐to‐nucleus signaling plays a central role in coordinating nuclear and plastid gene expression. The gun (genomes uncoupled) mutants of Arabidopsis have been used to demonstrate that Mg‐protoporphyrin (Mg‐Proto) acts as a plastid signal to repress the transcription of nuclear photosynthesis genes.1 It is unclear how Mg‐Proto triggers repression, but several components of this pathway have been recently identified. These include the products of GUN4 and GUN5. GUN5 is the ChlH subunit of Mg‐chelatase, which produces Mg‐Proto, and GUN4 is a (...) regulator of ChlH activity.2 GUN4 might also play a role in photoprotection and in the trafficking of Mg‐Proto. BioEssays 25:631–636, 2003. © 2003 Wiley Periodicals, Inc. (shrink)

Proteins are targeted to plastids by N‐terminal transit peptides, which are recognized by protein import complexes in the organelle membranes. Historically, transit peptide properties have been defined from vascular plant sequences, but recent large‐scale genome sequencing from the many plastid‐containing lineages across the tree of life has provided a much broader representation of targeted proteins. This includes the three lineages containing primary plastids (plants and green algae, rhodophytes and glaucophytes) and also the seven major lineages that contain secondary (...) plastids, “secondhand” plastids derived through eukaryotic endosymbiosis. Despite this extensive spread of plastids throughout Eukaryota, an N‐terminal transit peptide has been maintained as an essential plastid‐targeting motif. This article provides the first global comparison of transit peptide composition and summarizes conservation of some features, the loss of an ancestral motif from the green lineages including plants, and modifications to transit peptides that have occurred in secondary and even tertiary plastids. BioEssays 29:1048–1058, 2007. © 2007 Wiley Periodicals, Inc. (shrink)

What factors drove the transformation of the cyanobacterial progenitor of plastids (e.g. chloroplasts) from endosymbiont to bona fide organelle? This question lies at the heart of organelle genesis because, whereas intracellular endosymbionts are widespread in both unicellular and multicellular eukaryotes (e.g. rhizobial bacteria, Chlorella cells in ciliates, Buchnera in aphids), only two canonical eukaryotic organelles of endosymbiotic origin are recognized, the plastids of algae and plants and the mitochondrion. Emerging data on (1) the discovery of non‐canonical plastid protein (...) targeting, (2) the recent origin of a cyanobacterial‐derived organelle in the filose amoeba Paulinella chromatophora, and (3) the extraordinarily reduced genomes of psyllid bacterial endosymbionts begin to blur the distinction between endosymbiont and organelle. Here we discuss the use of these terms in light of new data in order to highlight the unique aspects of plastids and mitochondria and underscore their central role in eukaryotic evolution. BioEssays 29:1239–1246, 2007. © 2007 Wiley Periodicals, Inc. (shrink)

The fundamental Hennigian principle, grouping solely on synapomorphy, is seldom used in modern phylogenetics. In the submitted paper, we apply this principle in reanalyzing five datasets comprising 197 complete plastid genomes (plastomes). We focused on the latter because plastome-based DNA sequence data gained dramatic popularity in molecular systematics during the last decade. We show that pattern-cladistic analyses based on complete plastid genome sequences can successfully resolve affinities between plant taxa, simultaneously simplifying both the genomic and analytical frameworks of phylogenetic studies. (...) We developed “Matrix to Newick” (M2N), a program to represent the standard molecular alignment of plastid genomes in the form of trees or relationships directly. Thus, massive plastome-based DNA sequence data can be successfully represented in a relational form rather than as a standard molecular alignment. Application of methods of median supertree construction (the Average Consensus method has been used as an example in this study) or Maximum Parsimony analysis to relational representations of plastome sequence data may help systematist to avoid the complicated assumption-based frameworks of Maximum Likelihood or Bayesian phylogenetics that are most used today in massive plastid sequence data analyses. We also found that significant amounts of pure genomic information that typically accommodate the majority of current plastid phylogenomic studies can be effectively dropped by systematists if they focus on the pattern-cladistics or relational analyses of plastome-based molecular data. The proposed pattern-cladistic approach is a powerful and straightforward heuristic alternative to modern plastome-based phylogenetics. (shrink)

During evolution, the genomes of eukaryotic cells have undergone major restructuring to meet the new regulatory challenges associated with compartmentalization of the genetic material in the nucleus and the organelles acquired by endosymbiosis (mitochondria and plastids). Restructuring involved the loss of dispensable or redundant genes and the massive translocation of genes from the ancestral organelles to the nucleus. Genomics and bioinformatic data suggest that the process of DNA transfer from organelles to the nucleus still continues, providing raw material for (...) evolutionary tinkering in the nuclear genome. Recent reconstruction of these events in the laboratory has provided a unique tool to observe genome evolution in real time and to study the molecular mechanisms by which plastid genes are converted into functional nuclear genes. Here, we summarize current knowledge about plastid‐to‐nuclear gene transfer in the context of genome evolution and discuss new insights gained from experiments that recapitulate endosymbiotic gene transfer in the laboratory. BioEssays 30:556–566, 2008. © 2008 Wiley Periodicals, Inc. (shrink)

A flurry of recent publications have challenged consensus views on the tempo and mode of plastid (chloroplast) evolution in eukaryotes and, more generally, the impact of endosymbiosis in the evolution of the nuclear genome. Endosymbiont‐to‐nucleus gene transfer is an essential component of the transition from endosymbiont to organelle, but the sheer diversity of algal‐derived genes in photosynthetic organisms such as diatoms, as well as the existence of genes of putative plastid ancestry in the nuclear genomes of plastid‐lacking eukaryotes such as (...) ciliates and choanoflagellates, defy simple explanation. Collectively, these papers underscore the power of comparative genomics and, at the same time, reveal how little we know with certainty about the earliest stages of the evolution of photosynthetic eukaryotes. Editor's suggested further reading in BioEssaysEarly steps in plastid evolution: current ideas and controversies AbstractDinoflagellate mitochondrial genomes: stretching the rules of molecular biology Abstract. (shrink)

We hypothesize that as one of the most consequential events in evolution, primary endosymbiosis accelerates lineage divergence, a process we refer to as the endosymbiotic ratchet. Our proposal is supported by recent work on the photosynthetic amoeba, Paulinella, that underwent primary plastid endosymbiosis about 124 Mya. This amoeba model allows us to explore the early impacts of photosynthetic organelle (plastid) origin on the host lineage. The current data point to a central role for effective population size (Ne) in accelerating divergence (...) post‐endosymbiosis due to limits to dispersal and reproductive isolation that reduce Ne, leading to local adaptation. We posit that isolated populations exploit different strategies and behaviors and assort themselves in non‐overlapping niches to minimize competition during the early, rapid evolutionary phase of organelle integration. The endosymbiotic ratchet provides a general framework for interpreting post‐endosymbiosis lineage evolution that is driven by disruptive selection and demographic and population shifts. Also see the video abstract here: https://youtu.be/gYXrFM6Zz6Q. (shrink)

At first glance the three eukaryotic protein translocation machineries – the ER‐associated degradation (ERAD) transport apparatus of the endoplasmic reticulum, the peroxisomal importomer and SELMA, the pre‐protein translocator of complex plastids – appear quite different. However, mechanistic comparisons and phylogenetic analyses presented here suggest that all three translocation machineries share a common ancestral origin, which highlights the recycling of pre‐existing components as an effective evolutionary driving force.Editor's suggested further reading in BioEssays ERAD ubiquitin ligases Abstract.

Plastids and mitochondria arose through endosymbiotic acquisition of formerly free-living bacteria. During more than a billion years of subsequent concerted evolution, the three genomes of plant cells have undergone dramatic structural changes to optimize the expression of the compartmentalized genetic material and to fine-tune the communication between the nucleus and the organelles. The chimeric composition of many multiprotein complexes in plastids and mitochondria (one part of the subunits being nuclear encoded and another one being encoded in the organellar (...) genome) provides a paradigm for co-evolution at the cellular level. In this paper, we discuss the co-evolution of nuclear and organellar genomes in the context of environmental adaptation in species and populations. We highlight emerging genetic model systems and new experimental approaches that are particularly suitable to elucidate the molecular basis of co-adaptation processes and describe how nuclear-cytoplasmic co-evolution can cause genetic incompatibilities that contribute to the establishment of hybridization barriers, ultimately leading to the formation of new species. (shrink)

Chloroplasts and other plastids are plant cell organelles that account for major biochemical functions. They contain their own gene expression system but are integrated into the signaling network of the entire cell. Both nuclear and plastid genes are involved in chloroplast biogenesis, and the gene expression pathways both inside and outside the organelle are subject to developmental and environmental control. The plastid transcription apparatus reflects this general scheme, with a basic organelle‐encoded enzymatic machinery surrounded by factors that may be (...) encoded by nuclear genes. Among the transcription regulatory mechanisms thought to play a role during plastid development are: (1) differential usage of promoter elements; (2) phosphorylation of transcription factors by a protein kinase, which is itself subject to phosphorylation and redox control; (3) dynamic changes in the composition of the transcription apparatus. In etioplasts, the dominating polymerase ‘B’ is a bacterial‐type enzyme, whereas the major chloroplast polymerase ‘A’ is a much larger enzyme reminiscent of those in the nucleus. These two enzyme forms may share common components and recruit others during development. (shrink)

The model of major transitions in evolution devised by Maynard Smith and Szathmáry has exerted tremendous influence over evolutionary theorists. Although MTE has been criticized for inconsistently combining different types of event, its ongoing appeal lies in depicting hierarchical increases in complexity by means of evolutionary transitions in individuality. In this paper, we consider the implications of major evolutionary events overlooked by MTE and its ETI-oriented successors, specifically the biological oxygenation of Earth, and the acquisitions of mitochondria and plastids. (...) By reflecting on these missed events, we reveal a central philosophical disagreement over the explanatory goals of major transitions theory that has yet to be made explicit in the literature. We go on to argue that this philosophical disagreement is only reinforced by Szathmáry’s recent revisions of MTE in the form of MTE 2.0. This finding motivates us to propose an alternative explanatory strategy: specifically, an interactionist metabolic perspective on major transitions. A metabolic framework not only avoids many of the criticisms that beset classic and revised MTE models, but also accommodates missing events and provides crucial explanatory components for standard major transitions. Although we do not provide a full-blown alternative theory and do not claim to achieve unity, we explain why foregrounding metabolism is crucial for any attempt to capture the major turning points in evolution, and why it does not lead to unmanageable pluralism. (shrink)

The significance of horizontal gene transfer (HGT) in eukaryotic evolution remains controversial. Although many eukaryotic genes are of bacterial origin, they are often interpreted as being derived from mitochondria or plastids. Because of their fixed gene pool and gene loss, however, mitochondria and plastids alone cannot adequately explain the presence of all, or even the majority, of bacterial genes in eukaryotes. Available data indicate that no insurmountable barrier to HGT exists, even in complex multicellular eukaryotes. In addition, the (...) discovery of both recent and ancient HGT events in all major eukaryotic groups suggests that HGT has been a regular occurrence throughout the history of eukaryotic evolution. A model of HGT is proposed that suggests both unicellular and early developmental stages as likely entry points for foreign genes into multicellular eukaryotes. (shrink)

The photosynthetic organelle of algae and plants (the plastid) traces its origin to a primary endosymbiotic event in which a previously non‐photosynthetic protist engulfed and enslaved a cyanobacterium. This eukaryote then gave rise to the red, green and glaucophyte algae. However, many algal lineages, such as the chlorophyll c‐containing chromists, have a more complicated evolutionary history involving a secondary endosymbiotic event, in which a protist engulfed an existing eukaryotic alga (in this case, a red alga). Chromists such as diatoms and (...) kelps then rose to great importance in aquatic habitats. Another algal group, the dinoflagellates, has undergone tertiary (engulfment of a secondary plastid) and even quaternary endosymbioses. In this review, we examine algal diversity and show endosymbiosis to be a major force in algal evolution. This area of research has advanced rapidly and long‐standing issues such as the chromalveolate hypothesis and the extent of endosymbiotic gene transfer have recently been clarified. BioEssays 26:50–60, 2004. © 2003 Wiley Periodicals, Inc. (shrink)

The realization that prokaryotes naturally and frequently disperse genes across steep taxonomic boundaries via lateral gene transfer gave wings to the idea that eukaryotes might do the same. Eukaryotes do acquire genes from mitochondria and plastids and they do transfer genes during the process of secondary endosymbiosis, the spread of plastids via eukaryotic algal endosymbionts. From those observations it, however, does not follow that eukaryotes transfer genes either in the same ways as prokaryotes do, or to a quantitatively (...) similar degree. An important illustration of the difference is that eukaryotes do not exhibit pangenomes, though prokaryotes do. Eukaryotes reveal no detectable cumulative effects of LGT, though prokaryotes do. A critical analysis suggests that something is deeply amiss with eukaryote LGT theories. In prokaryotes, genes from the environment can enter the genome via lateral gene transfer. In eukaryote genetics, natural variation comes from within the genome, not from the environment. Yet many reports claim that eukaryotes undergo LGT just like prokaryotes. Such claims do not withstand scrutiny and are probably untrue. (shrink)

We use genomic information to tell us stories of evolutionary origins. But what does it mean when different genomes report wildly different accounts of lineage history? This genomic “discordance” can be a consequence of a fascinating suite of natural history and evolutionary phenomena, from the different inheritance mechanisms of nuclear versus cytoplasmic (mitochondrial and plastid) genomes to hybridization and introgression to horizontal transfer. Here, we explore how we can use these distinct genomic stories to provide new insights into the maintenance (...) of sexual reproduction, one of the most important unanswered questions in biology. We focus on the strikingly distinct nuclear versus mitochondrial versions of the story surrounding the origin and maintenance of asexual lineages in Potamopyrgus antipodarum, a New Zealand freshwater snail. While key questions remain unresolved, these data inspire multiple testable hypotheses that can be powerfully applied across a broad range of taxa toward a deeper understanding of the causes and consequences of mitonuclear discordance, the maintenance of sex, and the origin of new asexual lineages. (shrink)

According to scientific procedure, each discipline first describes the phenomena of its research area, then analyzes them, and tinally categorizes them in a system. To date, biology has lacked such a system for its smallest building blocks, the cells. Although the theory of evolution explains certain central evolutionary mechanisms of the cell, there existed no generally accepted theory of the organization of the cell. The endoeytobiotic cell theory is suggested as a possible basis for a satisfying explanation of the structure, (...) function, information, and evolution of the cell. Furthermore, a hypothetical periodic system of the cell is developed. This system consists of eight groups, including the ecological niches fermentation, respiration, photergy, and photosynthesis (each aerobic and anaerobic) and seven periods with increasing numbers of protein biosynthesis machineries (cytoplasma, mitochondria, plastids, endocytobionts). We find furthermore, a division according to typical animal or plant cells and between these two in fungus-like cells. (shrink)

The most common form of the CO2‐fixing enzyme rubisco is a form I enzyme, heretofore found universally in oxygenic phototrophs (cyanobacteria and plastids) and widely in proteobacteria. Two groups(1–4), however, now report that in dinoflagellate plastids the usual form I rubisco has been replaced by the distantly related form II enzyme, known previously only from anaerobic proteobacteria. This raises the important question of how such an oxygensensitive rubisco could function in an aerobic organism. Moreover, the dinoflagellate rubisco has (...) unusual molecular properties: it is encoded as a polyprotein, by nuclear (rather than plastid) genes, and these genes contain noncanonical spliceosomal introns. The nuclear location and alphaproteobacterial affinity of dinoflagellate rubisco genes hint at a possible mitochondrial origin and highlight the extraordinary richness of lateral gene transfers, both between and within organisms, that have occurred during rubisco evolution. (shrink)

Cytokinins are plant hormones which have long been associated with cell division and plastid differentiation. Recently, they have been found to play a central role also in the growth of plant tumors. Certain phytopathogenic bacteria, notably Agrobacterium tumefaciens and Pseudomonas syringae pv. savastanoi, can incite tumors on dicotyledonous plants and such tumors exhibit growth which is characteristic of the presence of excess auxin and cytokinin. Genes specifying cytokinin biosynthesis have now been isolated from both sets of bacteria. The genes encode (...) prenyl transferase responsible for cytokinin biosynthesis which, upon expression in E. coli,cause the production of the active cytokinin, zeatin. Expression of these genes in association with the plant is responsible for at least part of the tumor phenotype, although the molecular mechanisms of infection by these bacteria are apparently quite dissimilar. There is extensive homology between the cytokinin biosynthetic genes from the two sets of bacteria. (shrink)

Algae are significant members of Earth's biodiversity. Having been studied for a long time, the discovery of new algal phyla is extremely unusual. Recently, the enigmatic “Picobiliphyta,” a group of uncultured eukaryotes unveiled using molecular tools, were claimed to represent an unrecognized early branching algal lineage with a nucleomorph (remnant nucleus of a secondary algal endosymbiont) in their plastids. However, subsequent studies rejected the presence of a nucleomorph, and single‐cell genomic studies failed to detect any plastid‐related genes, ruling out (...) the possibility of plastid occurrence. The isolation of the first “picobiliphyte,” Picomonas judraskeda, a tiny organism that feeds on very small (<150 nm) organic particles, came as final proof of their non‐photosynthetic lifestyle. Consequently, the group has been renamed Picozoa. The passage from “picobiliphytes” to “picozoa” illustrates the crucial role that classical protistology should play to provide sound biological context for the wealth of data produced by modern molecular techniques. (shrink)

The cryptomonads and chlorarachniophytes are two unicellular algal lineages with complex cellular structures and fascinating evolutionary histories. Both groups acquired their photosynthetic abilities through the assimilation of eukaryotic endosymbionts. As a result, they possess two distinct cytosolic compartments and four genomes—two nuclear genomes, an endosymbiont‐derived plastid genome and a mitochondrial genome derived from the host cell. Like mitochondrial and plastid genomes, the genome of the endosymbiont nucleus, or ‘nucleomorph’, of cryptomonad and chlorarachniophyte cells has been greatly reduced through the combined (...) effects of gene loss and intracellular gene transfer. This article focuses on the structure, function, origin and evolution of cryptomonad and chlorarachniophyte nucleomorph genomes in light of recent comparisons of genome sequence data from both groups. It is now possible to speculate on the reasons that nucleomorphs persist in cryptomonads and chlorarachniophytes but have been lost in all other algae with plastids of secondary endosymbiotic origin. BioEssays 29:392–402, 2007. © 2007 Wiley Periodicals, Inc. (shrink)

The most interesting biological molecules are long polymers. In analogy with human alphabetic languages, they can be called texts and analysed, as to the primary structure, as sequences of letters or of words . It is considered that the study of words, in a linguistic approach, may contribute positively to the understanding of molecular interactions . The molecular and human languages and dialects are contrasted. The molecular one is peculiarly distinct from the human, for instance, by its use of a (...) tridimensional morphology, temporal dynamics, absence of spacings and punctuation, and overlapping messages. A mathematical method is presented, for discovering words in texts. The word AAA was studied in the evolution of the 5S ribosomal RNA. It was shown that this word is more frequent in less complex organisms and less frequent in the more complex ones, in the fungi, plants, and vertebrates lineages. In the two latter ones, the degree of genie variability was also reduced. To the contrary, a moderate degree of usage of this word persisted in the whole invertebrates lineage, where a high degree of genie variability was maintained. In mitochondria, plastids and mycoplasmas, the frequency of the word AAA was increased, consistently with their need for interactions with a wider range of variation. These behaviors indicate that the monotonous AAA word allows for ambiguity in interactions. With the evolution of organic complexity and of greater molecular specificity, ambiguous words were progressively avoided.As moléculas biológicas mais interessantes são longos polímeros. Em analogia com a linguagem humana alfabética, estes podem ser chamados de textos, e analisados, quanto à estrutura primária, como sequência de letras ou de palavras . Considera-se que o estudo das palavras, em abordagem de tipo lingüístico, possa contribuir para o entendimento das interações moleculares. As linguagens e dialetos, moleculares e humanos, são contrastados. A linguagem molecular se distingue peculiarmente da humana, por exemplo, por utilizar forma tridimensional, dinâmica temporal, ausência de espaçamento e pontuação, e sobreposição de significados. Apresenta-se um método matemático para descoberta, de palavras em textos. A palavra AAA foi estudada na evolução do RNA ribossômico 5S. Observou-se que esta palavra é mais freqüente em organismos menos complexos e menos freqüente nos mais complexos, das linhagens de fungos, plantas e vertebrados. Nas duas últimas, reduziu-se também o grau de variabilidade gênica. Pelo contrário, grau moderado de freqüência da palavra persistiu em toda a linhagem dos invertebrados, com manutenção paralela de alto nível de variabilidade gênica. Nas mitocôndrias, plastídeos e micoplasmas, a freqüência da palavra AAA foi aumentada, de acordo com sua necessidade de interações com maior amplitude de variação. Esses comportamentos indicam que a palavra monótona AAA permite ambigüidade de interações. Com a evolução da complexidade orgânica e da maior especificidade molecular, as palavras ambíguas foram progressivamente evitadas. (shrink)

Mitochondria have been fundamental to the eco‐physiological success of eukaryotes since the last eukaryotic common ancestor (LECA). They contribute essential functions to eukaryotic cells, above and beyond classical respiration. Mitochondria interact with, and complement, metabolic pathways occurring in other organelles, notably diversifying the chloroplast metabolism of photosynthetic organisms. Here, we integrate existing literature to investigate how mitochondrial metabolism varies across the landscape of eukaryotic evolution. We illustrate the mitochondrial remodelling and proteomic changes undergone in conjunction with major evolutionary transitions. We (...) explore how the mitochondrial complexity of the LECA has been remodelled in specific groups to support subsequent evolutionary transitions, such as the acquisition of chloroplasts in photosynthetic species and the emergence of multicellularity. We highlight the versatile and crucial roles played by mitochondria during eukaryotic evolution, extending from its huge contribution to the development of the LECA itself to the dynamic evolution of individual eukaryote groups, reflecting both their current ecologies and evolutionary histories. (shrink)

In the organelles of plants and mammals, recent evidence suggests that genomic instability stems in large part from template switching events taking place during DNA replication. Although more than one mechanism may be responsible for this, some similarities exist between the different proposed models. These can be separated into two main categories, depending on whether they involve a single‐strand‐switching or a reciprocal‐strand‐switching event. Single‐strand‐switching events lead to intermediates containing Y junctions, whereas reciprocal‐strand‐switching creates Holliday junctions. Common features in all the (...) described models include replication stress, fork stalling and the presence of inverted repeats, but no single element appears to be required in all cases. We review the field, and examine the ideas that several mechanisms may take place in any given genome, and that the presence of palindromes or inverted repeats in certain regions may favor specific rearrangements. (shrink)