The endosymbiotic origin,diversification and fate of plastids

Plastids and mitochondria each arose from a single endosymbiotic event and share many similarities in how they were reduced and integrated with their host. However, the subsequent evolution of the two organelles could hardly be more different: mitochondria are a stable fixture of eukaryotic cells that are neither lost nor shuffled between lineages, whereas plastid evolution has been a complex mix of movement, loss and replacement. Molecular data from the past decade have substantially untangled this complex history, and we now know that plastids are derived from a single endosymbiotic event in the ancestor of glaucophytes, red algae and green algae (including plants). The plastids of both red algae and green algae were subsequently transferred to other lineages by secondary endosymbiosis. Green algal plastids were taken up by euglenids and chlorarachniophytes, as well as one small group of dinoflagellates. Red algae appear to have been taken up only once, giving rise to a diverse group called chromalveolates. Additional layers of complexity come from plastid loss, which has happened at least once and probably many times, and replacement. Plastid loss is difficult to prove, and cryptic, non-photosynthetic plastids are being found in many non-photosynthetic lineages. In other cases, photosynthetic lineages are now understood to have evolved from ancestors with a plastid of different origin, so an ancestral plastid has been replaced with a new one. Such replacement has taken place in several dinoflagellates (by tertiary endosymbiosis with other chromalveolates or serial secondary endosymbiosis with a green alga), and apparently also in two rhizarian lineages: chlorarachniophytes and Paulinella (which appear to have evolved from chromalveolate ancestors). The many twists and turns of plastid evolution each represent major evolutionary transitions, and each offers a glimpse into how genomes evolve and how cells integrate through gene transfers and protein trafficking.     

Protein Phylogenies and Signature Sequences: A Reappraisal of Evolutionary Relationships among Archaebacteria, Eubacteria, and Eukaryotes

The presence of shared conserved insertion or deletions (indels) in protein sequences is a special type of signature sequence that shows considerable promise for phylogenetic inference. An alternative model of microbial evolution based on the use of indels of conserved proteins and the morphological features of prokaryotic organisms is proposed. In this model, extant archaebacteria and gram-positive bacteria, which have a simple, single-layered cell wall structure, are termed monoderm prokaryotes. They are believed to be descended from the most primitive organisms. Evidence from indels supports the view that the archaebacteria probably evolved from gram-positive bacteria, and I suggest that this evolution occurred in response to antibiotic selection pressures. Evidence is presented that diderm prokaryotes (i.e., gram-negative bacteria), which have a bilayered cell wall, are derived from monoderm prokaryotes. Signature sequences in different proteins provide a means to define a number of different taxa within prokaryotes (namely, low G+C and high G+C gram-positive, Deinococcus-Thermus, cyanobacteria, chlamydia-cytophaga related, and two different groups of Proteobacteria) and to indicate how they evolved from a common ancestor. Based on phylogenetic information from indels in different protein sequences, it is hypothesized that all eukaryotes, including amitochondriate and aplastidic organisms, received major gene contributions from both an archaebacterium and a gram-negative eubacterium. In this model, the ancestral eukaryotic cell is a chimera that resulted from a unique fusion event between the two separate groups of prokaryotes followed by integration of their genomes.     

The place of viruses in the "tree of life"

Ribozymal entry into vesicle containing autocatalytically replicating oligopeptides engendered RNA proliferation and enzyme synthesis within units whose RNA genomes derived from ancestors of viroids. There is good reason to consider the coexistence of proto- or spheroplastic forms of ancient prokaryotes and archaeons. Predecessors of extant mycoplasmavirus L3 or archaeal fuselloviruses could induce cell fusions among these entities. The possibility that the first eukaryotic cells arose consequentially to virally mediated fusions of prokaryotic and archaeal proto- or spheroplasts is presented. Retrotransposons and endogenous retroviruses might have emerged in theropod dinosaurs when Aves evolved; and directed the development of syncytiotrophoblasts in the placentae of the first mammals. As viruses coevolved with their hosts descendants of ancient viruses diverged from one another. Certain phenotypical features could connect extant phages and eukaryotic viruses to common ancestors.     

Inferring the biogeographic origins of inter‐continental disjunct endemics using a Bayes‐DIVA approach

The arcto‐Tertiary relictual flora is comprised of many genera that occur non‐contiguously in the temperate zones of eastern Asia, Europe, eastern North America, and western North America. Within each distributional area, species are typically endemic and may thus be widely separated from closely related species within the other areas. It is widely accepted that this common pattern of distribution resulted from of the fragmentation of a once more‐continuous arcto‐Tertiary forest. The historical biogeographic events leading to the present‐day disjunction have often been investigated using a phylogenetic approach. Limitations to these previous studies have included phylogenetic uncertainty and uncertainty in ancestral range reconstructions. However, the recently described Bayes‐DIVA method handles both types of uncertainty. Thus, we used Bayes‐DIVA analysis to reconstruct the stem lineage distributions for 185 endemic lineages from 23 disjunct genera representing 17 vascular plant families. In particular, we asked whether endemic lineages within each of the four distributional areas more often evolved from (1) widespread ancestors, (2) ancestors dispersed from other areas, or (3) endemic ancestors. We also considered which of these three biogeographic mechanisms may best explain the origins of arcto‐Tertiary disjunct endemics in the neotropics. Our results show that eastern Asian endemics more often evolved from endemic ancestors compared to endemics in Europe and eastern and western North America. Present‐day endemic lineages in the latter areas more often arose from widespread ancestors. Our results also provide anecdotal evidence for the importance of dispersal in the biogeographic origins of arcto‐Tertiary species endemic in the neotropics.     

Genome size of chrysophytes varies with cell size and nutritional mode

The cellular content of nuclear DNA varies up to 200,000-fold between eukaryotes. These differences can arise via different mechanisms. In particular, cell size and nutritional mode may influence evolution of the nuclear DNA content. Chrysophytes comprise organisms with different cell organizations and nutritional modes. Heterotrophic clades evolved independently several times from phototrophic or mixotrophic ancestors. Thus, chrysophytes are an ideal model taxon for investigating the effect of the nutritional mode on cellular DNA content. We investigated the genome size of heterotrophic, mixotrophic, and phototrophic chrysophytes. We demonstrate that cell sizes and genome sizes differ significantly between taxa with different nutritional modes. Phototrophic strains tend to have larger cell volumes and larger genomes than heterotrophic strains do. The investigated mixotrophic strains had intermediate cell volumes and small to intermediate genome sizes. Heterotrophic chrysophytes had the smallest genomes and cell volumes compared to other chrysophytes. In general, genome size increased with cell volume, but cell volume only partially explained the variation in genome size. In particular, genome sizes of mixotrophic strains were smaller than expected based on cell sizes.     

Analysis of evolution of exon-intron structure of eukaryotic genes

The availability of multiple, complete eukaryotic genome sequences allows one to address many fundamental evolutionary questions on genome scale. One such important, long-standing problem is evolution of exon-intron structure of eukaryotic genes. Analysis of orthologous genes from completely sequenced genomes revealed numerous shared intron positions in orthologous genes from animals and plants and even between animals, plants and protists. The data on shared and lineage-specific intron positions were used as the starting point for evolutionary reconstruction with parsimony and maximum-likelihood approaches. Parsimony methods produce reconstructions with intron-rich ancestors but also infer lineage-specific, in many cases, high levels of intron loss and gain. Different probabilistic models gave opposite results, apparently depending on model parameters and assumptions, from domination of intron loss, with extremely intron-rich ancestors, to dramatic excess of gains, to the point of denying any true conservation of intron positions among deep eukaryotic lineages. Development of models with adequate, realistic parameters and assumptions seems to be crucial for obtaining more definitive estimates of intron gain and loss in different eukaryotic lineages. Many shared intron positions were detected in ancestral eukaryotic paralogues which evolved by duplication prior to the divergence of extant eukaryotic lineages. These findings indicate that numerous introns were present in eukaryotic genes already at the earliest stages of evolution of eukaryotes and are compatible with the hypothesis that the original, catastrophic intron invasion accompanied the emergence of the eukaryotic cells. Comparison of various features of old and younger introns starts shedding light on probable mechanisms of intron insertion, indicating that propagation of old introns is unlikely to be a major mechanism for origin of new ones. The existence and structure of ancestral protosplice sites were addressed by examining the context of introns inserted within codons that encode amino acids conserved in all eukaryotes and, accordingly, are not subject to selection for splicing efficiency. It was shown that introns indeed predominantly insert into or are fixed in specific protosplice sites which have the consensus sequence (A/C)AG|Gt.     

Enslaved bacteria as new hope for plant biotechnologists

The most distinguishing feature of the plant cell is a DNA-containing organelle that sets plants apart from all other organisms: the chloroplast. Compelling evidence supports an endosymbiotic origin for chloroplasts. According to this theory, chloroplasts are descendants of formerly free-living cyanobacterial ancestors which entered an endosymbiotic relationship with a pre-eukaryotic cell and were ultimately integrated into the metabolism of the host cell. Chloroplasts retain many prokaryotic features and their gene expression system still closely resembles that of their eubacterial ancestors. During the past decade, our knowledge about chloroplast biology has benefited immensely from a most remarkable methodological breakthrough: the development of transformation technologies for chloroplast genomes. Moreover, recent advances in the manipulation of higher plant chloroplast genomes have created unprecedented opportunities for the genetic engineering of plants and promise to overcome many of the problems associated with conventional transgenic technologies. This review describes the state of the art in genetic engineering of higher plant chloroplast genomes and highlights the tremendous potential of these technologies for the biotechnology of the future. Received: 27 January 2000 / Received revision: 15 March 2000 / Accepted: 24 March 2000     

Retention and loss of amino acid biosynthetic pathways based on analysis of whole-genome sequences

Plants and fungi can synthesize each of the 20 amino acids by using biosynthetic pathways inherited from their bacterial ancestors. However, the ability to synthesize nine amino acids (Phe, Trp, Ile, Leu, Val, Lys, His, Thr, and Met) was lost in a wide variety of eukaryotes that evolved the ability to feed on other organisms. Since the biosynthetic pathways and their respective enzymes are well characterized, orthologs can be recognized in whole genomes to understand when in evolution pathways were lost. The pattern of pathway loss and retention was analyzed in the complete genomes of three early-diverging protist parasites, the amoeba Dictyostelium, and six animals. The nine pathways were lost independently in animals, Dictyostelium, Leishmania, Plasmodium, and Cryptosporidium. Seven additional pathways appear to have been lost in one or another parasite, demonstrating that they are dispensable in a nutrition-rich environment. Our predictions of pathways retained and pathways lost based on computational analyses of whole genomes are validated by minimal-medium studies with mammals, fish, worms, and Dictyostelium. The apparent selective advantages of retaining biosynthetic capabilities for amino acids available in the diet are considered.     

Ontogenetic mechanisms and the evolution of Cactaceae

Abstract

The ancestors of cacti were leafy trees that had hard, woody trunks. The development of the cactus body is controlled by ontogenetic mechanisms that have evolved, and now they produce a body that is leafless, succulent and has a photosynthetic cortex. Specific changes include: bark formation is postponed and the epidermis and stomata function for many years; the outer cortex is a palisade cortex with intercellular spaces; there are cortical bundles that resemble leaf veins but which have secondary xylem and phloem. Wood development has changed dramatically such that water storage is maximized (increased ray parenchyma) and danger of water stress is minimized (increased paratracheal parenchyma, loss of fibers). Several genera have polymorphic wood: the plants produce one type of wood for several years, then later they produce a different type. It is possible that the extensive evolutionary changes have resulted from mutations in the controller regions of genes, not in the structural regions.     

Genetic variability and adaptive evolution in parthenogenetic root-knot nematodes

Root-knot nematodes (RKN) of the genus Meloidogyne are biotrophic plant parasites of major agricultural importance, which exhibit very variable modes of reproduction, from classical amphimixis to mitotic parthenogenesis. This review focuses on those RKN species that reproduce exclusively by mitotic parthenogenesis (apomixis), in contrast to those that have meiotic/amphimitic events in their life cycle. Although populations of clonal organisms are often represented as being ecologically isolated and evolutionary inert, a considerable volume of literature provides evidence that asexual RKN are neither: they are widely distributed, extremely polyphagous, and amenable to selection and adaptive variation. The ancestors of the genus are unknown, but it is assumed that the parthenogenetic RKN have evolved from amphimictic species through hybridization and subsequent aneuploidization and polyploidization events. Molecular studies have indeed confirmed that the phylogenetic divergence between meiotic and mitotic RKN lineages occurred early, and have revealed an unexpected level of clonal diversity among populations within apomictic species. Laboratory experiments have shown that asexual RKN can rapidly adapt to new environmental constraints (eg host resistance), although with some fitness costs. Lastly, the molecular and chromosomal mechanisms that could contribute to genome plasticity leading to persistent genetic variation and adaptive evolution in apomictic RKN are discussed. It is concluded that RKN provide an excellent model system in which to study the dynamic nature and adaptive potential of clonal genomes.     

In silico archeogenomics unveils modern plant genome organisation, regulation and evolution

Increasing access to plant genome sequences as well as high resolution gene-based genetic maps have recently offered the opportunity to compare modern genomes and model their evolutionary history from their reconstructed founder ancestors on an unprecedented scale. In silico paleogenomic data have revealed the evolutionary forces that have shaped present-day genomes and allowed us to gain insight into how they are organised and regulated today.     

Reconstruction of ancient genome and gene order from complete microbial genome sequences

Microbial genome sequences provide us with the fossil records for inferring their origination and evolution. Assuming that current microbial genomes are the evolutionary results of ancient genomes or fragments and the neighboring genes in ancient genomes are more likely neighbors in current genomes, in this paper we proposed a paleontological algorithm and assembled the orthologous gene groups from 66 complete and current microbial genome sequences into a pseudo-ancient genome, which consists of continuous fragments of various sizes. We performed bootstrap resampling and correlation analyses and the results showed that the assembled ancient genome and fragments are statistically significant and the genes of the same fragment are inherently related and likely derived from common ancestors. This method provides a new computational tool for studying microbial genome structure and evolution.     

Phylogeny and sex chromosome evolution of Palaeognathae

Many paleognaths (ratites and tinamous) have a pair of homomorphic ZW sex chromosomes in contrast to the highly differentiated sex chromosomes of most other birds. To understand the evolutionary causes for the different tempos of sex chromosome evolution, we produced female genomes of 12 paleognathous species and reconstructed the phylogeny and the evolutionary history of paleognathous sex chromosomes. We uncovered that Palaeognathae sex chromosomes had undergone stepwise recombination suppression and formed a pattern of “evolutionary strata”. Nine of the 15 studied species' sex chromosomes have maintained homologous recombination in their long pseudoautosomal regions extending more than half of the entire chromosome length. We found that in the older strata, the W chromosome suffered more serious functional gene loss. Their homologous Z-linked regions, compared with other genomic regions, have produced an excess of species-specific autosomal duplicated genes that evolved female-specific expression, in contrast to their broadly expressed progenitors. We speculate such “defeminization” of Z chromosome with underrepresentation of female-biased genes and slow divergence of sex chromosomes of paleognaths might be related to their distinctive mode of sexual selection targeting females rather than males, which evolved in their common ancestors.     

Recycled plastids: a 'green movement' in eukaryotic evolution

Secondary endosymbiosis is the process that drives the spread of plastids (chloroplasts) from one eukaryote to another. The number of times that this has occurred and the kinds of cells involved are now becoming clear. Reconstructions of plastid history using molecular data suggest that secondary endosymbiosis is very rare and that perhaps as few as three endosymbioses have resulted in a large proportion of algal diversity. The significance of these events extends beyond photosynthesis, however, because non-photosynthetic organisms such as ciliates appear to have evolved from photosynthetic ancestors and could still harbor plastid-derived genes or relict plastids.     

Paleogenomics in vertebrates, or the recovery of lost genomes from the mist of time

Knowledge of the structure of ancestral genomes provides the basis of a new framework to better represent and interpret results from genomic and evolutionary studies. Because these ancestors lived tens of hundreds of million years ago, this knowledge will inevitably take the form of abstract representations, reconstructed on the basis both of experimental evidence collected on extant genomes and of our understanding of evolutionary processes. This is the field of Paleogenomics, a young discipline that is providing an increasingly precise picture of our ancestral vertebrate genomes based on cytogenetic data, genome sequences and new algorithmic developments. Many recent studies have focused on the ancestral placental mammal and teleost fish genomes, although the outlines of even more distant pre-vertebrate ancestors are being reported.     

The behavior and the morphology of sea lilies with shortened stalks: implications on the evolution of feather stars

Extant crinoids can be divided into two groups, stalked sea lilies and stalkless feather stars. Feather stars are considered to have evolved from stalked ancestors by losing most of the stalk, but other differences are present between the two groups. The unsegmented centrodorsal, long and curved cirri near the crown, small calyx, and the ability to swim are all feather star features not found in the sea lilies. To figure out which of the above features evolved directly correlating with loss of the stalk in feather stars, we cut off the stalk from the sea lily Metacrinus rotundus and kept them alive in an aquarium. The specimens with shortened stalks were able to stand and crawl with their arms without the support of their stalks, but swimming was not observed for any of the animals. Morphologically, neither fusion of the remaining segments nor the reduction of the size of the calyx were observed, but the cirri became long and curved near the crown. Therefore, the extant sea lilies possess a potential to adapt to incidents of stalk loss. Specimens autotomizing most of their stalks were observed, suggesting that the potential is actually employed in nature. This mechanism linking the reduction of the stalk and the changes in the morphology of cirri may have played an important role in the evolution of the feather stars, if the stalked ancestors of feather stars also possessed this potential. Experimental zoological approaches as this study may provide new insights to the questions of evolution.     

Carbonic anhydrase and the molecular evolution of C4 photosynthesis

C(4) photosynthesis, a biochemical CO(2)-concentrating mechanism (CCM), evolved more than 60 times within the angiosperms from C(3) ancestors. The genus Flaveria, which contains species demonstrating C(3), C(3)-C(4), C(4)-like or C(4) photosynthesis, is a model for examining the molecular evolution of the C(4) pathway. Work with carbonic anhydrase (CA), and C(3) and C(4) Flaveria congeners has added significantly to the understanding of this process. The C(4) form of CA3, a β-CA, which catalyses the first reaction in the C(4) pathway by hydrating atmospheric CO(2) to bicarbonate in the cytosol of mesophyll cells (mcs), evolved from a chloroplastic C(3) ancestor. The molecular modifications to the ancestral CA3 gene included the loss of the sequence encoding the chloroplast transit peptide, and mutations in regulatory regions that resulted in high levels of expression in the C(4) mesophyll. Analyses of the CA3 proteins and regulatory elements from Flaveria photosynthetic intermediates indicated C(4) biochemistry very likely evolved in a specific, stepwise manner in this genus. The details of the mechanisms involved in the molecular evolution of other C(4) plant β-CAs are unknown; however, comparative genetics indicate gene duplication and neofunctionalization played significant roles as they did in Flaveria.     

Origin and evolution of spliceosomal introns

ABSTRACT: Evolution of exon-intron structure of eukaryotic genes has been a matter of long-standing, intensive debate. The introns-early concept, later rebranded 'introns first' held that protein-coding genes were interrupted by numerous introns even at the earliest stages of life's evolution and that introns played a major role in the origin of proteins by facilitating recombination of sequences coding for small protein/peptide modules. The introns-late concept held that introns emerged only in eukaryotes and new introns have been accumulating continuously throughout eukaryotic evolution. Analysis of orthologous genes from completely sequenced eukaryotic genomes revealed numerous shared intron positions in orthologous genes from animals and plants and even between animals, plants and protists, suggesting that many ancestral introns have persisted since the last eukaryotic common ancestor (LECA). Reconstructions of intron gain and loss using the growing collection of genomes of diverse eukaryotes and increasingly advanced probabilistic models convincingly show that the LECA and the ancestors of each eukaryotic supergroup had intron-rich genes, with intron densities comparable to those in the most intron-rich modern genomes such as those of vertebrates. The subsequent evolution in most lineages of eukaryotes involved primarily loss of introns, with only a few episodes of substantial intron gain that might have accompanied major evolutionary innovations such as the origin of metazoa. The original invasion of self-splicing Group II introns, presumably originating from the mitochondrial endosymbiont, into the genome of the emerging eukaryote might have been a key factor of eukaryogenesis that in particular triggered the origin of endomembranes and the nucleus. Conversely, splicing errors gave rise to alternative splicing, a major contribution to the biological complexity of multicellular eukaryotes. There is no indication that any prokaryote has ever possessed a spliceosome or introns in protein-coding genes, other than relatively rare mobile self-splicing introns. Thus, the introns-first scenario is not supported by any evidence but exon-intron structure of protein-coding genes appears to have evolved concomitantly with the eukaryotic cell, and introns were a major factor of evolution throughout the history of eukaryotes. This article was reviewed by I. King Jordan, Manuel Irimia (nominated by Anthony Poole), Tobias Mourier (nominated by Anthony Poole), and Fyodor Kondrashov. For the complete reports, see the Reviewers' Reports section.     

Cytosolic enzymes with a mitochondrial ancestry from the anaerobic chytrid Piromyces sp. E2

The anaerobic chytrid Piromyces sp. E2 lacks mitochondria, but contains hydrogen-producing organelles, the hydrogenosomes. We are interested in how the adaptation to anaerobiosis influenced enzyme compartmentalization in this organism. Random sequencing of a cDNA library from Piromyces sp. E2 resulted in the isolation of cDNAs encoding malate dehydrogenase, aconitase and acetohydroxyacid reductoisomerase. Phylogenetic analysis of the deduced amino acid sequences revealed that they are closely related to their mitochondrial homologues from aerobic eukaryotes. However, the deduced sequences lack N-terminal extensions, which function as mitochondrial leader sequences in the corresponding mitochondrial enzymes from aerobic eukaryotes. Subcellular fractionation and enzyme assays confirmed that the corresponding enzymes are located in the cytosol. As anaerobic chytrids evolved from aerobic, mitochondria-bearing ancestors, we suggest that, in the course of the adaptation from an aerobic to an anaerobic lifestyle, mitochondrial enzymes were retargeted to the cytosol with the concomitant loss of their N-terminal leader sequences.