Nonsense-Mediated Decay Enables Intron Gain in Drosophila

Intron number varies considerably among genomes, but despite their fundamental importance, the mutational mechanisms and evolutionary processes underlying the expansion of intron number remain unknown. Here we show that Drosophila, in contrast to most eukaryotic lineages, is still undergoing a dramatic rate of intron gain. These novel introns carry significantly weaker splice sites that may impede their identification by the spliceosome. Novel introns are more likely to encode a premature termination codon (PTC), indicating that nonsense-mediated decay (NMD) functions as a backup for weak splicing of new introns. Our data suggest that new introns originate when genomic insertions with weak splice sites are hidden from selection by NMD. This mechanism reduces the sequence requirement imposed on novel introns and implies that the capacity of the spliceosome to recognize weak splice sites was a prerequisite for intron gain during eukaryotic evolution.     

Fluidity of eukaryotic genomes

The understanding the different kinds of sequences that make up a genome, as well as their proportions in genomes (obtained by the sequencing of the complete genome), has considerably changed our idea of evolution at the genomic level. The former view of a slowly evolving genome has given way to the idea of a genome that can undergo many transformations, on a large or small scale, depending on the evolution of the different types of sequences constituting it. Here we summarise the evolution of these sequences and the impact it can have on the genome. We have focused on micro-transformations, and especially on the impact of transposable elements on genomes. To cite this article: E. Bonnivard, D. Higuet, C. R. Biologies 332 (2009).     

“Changing by doubling”, the impact of Whole Genome Duplications in the evolution of eukaryotes

Species are usually defined by reproductive isolation and are characterized by their gene repertoire. These two aspects are consequences of events fixed during evolution, including whole genome duplications and other polyploidizations. Thanks to the recent progress in genome sequencing, new light has been shed on these events. In this review, we will summarize these findings and discuss the methodology involved. Evolutionary traces of such events have been evidenced in various lineages in plants, animals, fungi and protozoa. Comparative analysis of synteny is a powerful approach to unveil evolutionary footprints of these events. According to expectations, these events would facilitate speciation since some of them are thought to be at the base of major radiations such as teleostei or eudicotyledons. After an initial amplification, the gene repertoire would be shaped by constraints such as expression level and functional interactions that would tend to maintain only a tiny fraction of the duplicates over the long term. Functional innovation from duplication may be a secondary effect, enabled by these duplicate retention mechanisms. To cite this article: O. Jaillon et al., C. R. Biologies 332 (2009).     

CircPlant:An Integrated Tool for circRNA Detection and Functional Prediction in Plants

The recent discovery of circular RNAs (circRNAs) and characterization of their functional roles have opened a new avenue for understanding the biology of genomes. circRNAs have been implicated to play important roles in a variety of biological processes, but their precise functions remain largely elusive. Currently, a few approaches are available for novel circRNA prediction, but almost all these methods are intended for animal genomes. Considering that the major differences between the organization of plant and mammal genomes cannot be neglected, a plant-specific method is needed to enhance the validity of plant circRNA identification. In this study, we present CircPlant, an integrated tool for the exploration of plant circRNAs, potentially acting as competing endogenous RNAs (ceRNAs), and their potential functions. With the incorporation of several unique plant-specific criteria, CircPlant can accurately detect plant circRNAs from high-throughput RNA-seq data. Based on comparison tests on simulated and real RNA-seq datasets from Arabidopsis thaliana and Oryza sativa, we show that CircPlant outperforms all evaluated competing tools in both accuracy and efficiency. CircPlant is freely available at http://bis.zju.edu.cn/circplant.     

Rapid evolution of enormous, multichromosomal genomes in flowering plant mitochondria with exceptionally high mutation rates

Genome size and complexity vary tremendously among eukaryotic species and their organelles. Comparisons across deeply divergent eukaryotic lineages have suggested that variation in mutation rates may explain this diversity, with increased mutational burdens favoring reduced genome size and complexity. The discovery that mitochondrial mutation rates can differ by orders of magnitude among closely related angiosperm species presents a unique opportunity to test this hypothesis. We sequenced the mitochondrial genomes from two species in the angiosperm genus Silene with recent and dramatic accelerations in their mitochondrial mutation rates. Contrary to theoretical predictions, these genomes have experienced a massive proliferation of noncoding content. At 6.7 and 11.3 Mb, they are by far the largest known mitochondrial genomes, larger than most bacterial genomes and even some nuclear genomes. In contrast, two slowly evolving Silene mitochondrial genomes are smaller than average for angiosperms. Consequently, this genus captures approximately 98% of known variation in organelle genome size. The expanded genomes reveal several architectural changes, including the evolution of complex multichromosomal structures (with 59 and 128 circular-mapping chromosomes, ranging in size from 44 to 192 kb). They also exhibit a substantial reduction in recombination and gene conversion activity as measured by the relative frequency of alternative genome conformations and the level of sequence divergence between repeat copies. The evolution of mutation rate, genome size, and chromosome structure can therefore be extremely rapid and interrelated in ways not predicted by current evolutionary theories. Our results raise the hypothesis that changes in recombinational processes, including gene conversion, may be a central force driving the evolution of both mutation rate and genome structure.     

The Tvv1 retrotransposon family is conserved between plant genomes separated by over 100 million years

Key message

Combining several different approaches, we have examined the structure, variability, and distribution of Tvv1 retrotransposons. Tvv1 is an unusual example of a low-copy retrotransposon metapopulation dispersed unevenly among very distant species and is promising for the development of molecular markers.

Abstract

Retrotransposons are ubiquitous throughout the genomes of the vascular plants, but individual retrotransposon families tend to be confined to the level of plant genus or at most family. This restricts the general applicability of a family as molecular markers. Here, we characterize a new plant retrotransposon named Tvv1_Sdem, a member of the Copia superfamily of LTR retrotransposons, from the genome of the wild potato Solanum demissum. Comparative analyses based on structure and sequence showed a high level of similarity of Tvv1_Sdem with Tvv1-VB, a retrotransposon previously described in the grapevine genome Vitis vinifera. Extending the analysis to other species by in silico and in vitro approaches revealed the presence of Tvv1 family members in potato, tomato, and poplar genomes, and led to the identification of full-length copies of Tvv1 in these species. We were also able to identify polymorphism in UTL sequences between Tvv1_Sdem copies from wild and cultivated potatoes that are useful as molecular markers. Combining different approaches, our results suggest that the Tvv1 family of retrotransposons has a monophyletic origin and has been maintained in both the rosids and the asterids, the major clades of dicotyledonous plants, since their divergence about 100 MYA. To our knowledge, Tvv1 represents an unusual plant retrotransposon metapopulation comprising highly similar members disjointedly dispersed among very distant species. The twin features of Tvv1 presence in evolutionarily distant genomes and the diversity of its UTL region in each species make it useful as a source of robust molecular markers for diversity studies and breeding.     

Subgenomic RNAs: The Possible Building Blocks for Modular Recombination ofClosteroviridaeGenomes

TheClosteroviridaeinclude several plant viruses of considerable economic importance, with unusually large positive-strand genomes of up to 20 kb. Molecular characterization of several of these viruses has now confirmed their coherent and unique position among the elongated plant RNA viruses. Structural comparisons of their genomes suggested a modular composition. The recent finding of multiple species of citrus tristeza virus (CTV) defective-RNAs, which have apparently resulted from the recombination of a subgenomic (sg)RNA, with distant parts from the 5′ end of the CTV genome, suggests thatClosteroviridaeare probably able to utilize sgRNAs and/or their promoter signals as factors for the modular exchange and rearrangement of their genomes.     

Recovery of 197 eukaryotic bins reveals major challenges for eukaryote genome reconstruction from terrestrial metagenomes

As most eukaryotic genomes are yet to be sequenced, the mechanisms underlying their contribution to different ecosystem processes remain untapped. Although approaches to recovering Prokaryotic genomes have become common in genome biology, few studies have tackled the recovery of eukaryotic genomes from metagenomes. This study assessed the reconstruction of microbial eukaryotic genomes using 6000 metagenomes from terrestrial and some transition environments using the EukRep pipeline. Only 215 metagenomic libraries yielded eukaryotic bins. From a total of 447 eukaryotic bins recovered 197 were classified at the phylum level. Streptophytes and fungi were the most represented clades with 83 and 73 bins, respectively. More than 78% of the obtained eukaryotic bins were recovered from samples whose biomes were classified as host-associated, aquatic, and anthropogenic terrestrial. However, only 93 bins were taxonomically assigned at the genus level and 17 bins at the species level. Completeness and contamination estimates were obtained for a total of 193 bins and consisted of 44.64% (σ = 27.41%) and 3.97% (σ = 6.53%), respectively. Micromonas commoda was the most frequent taxon found while Saccharomyces cerevisiae presented the highest completeness, probably because more reference genomes are available. Current measures of completeness are based on the presence of single-copy genes. However, mapping of the contigs from the recovered eukaryotic bins to the chromosomes of the reference genomes showed many gaps, suggesting that completeness measures should also include chromosome coverage. Recovering eukaryotic genomes will benefit significantly from long-read sequencing, development of tools for dealing with repeat-rich genomes, and improved reference genomes databases.     

SVA Retrotransposons and a Low Copy Repeat in Humans and Great Apes: A Mobile Connection

Segmental duplications (SDs) constitute a considerable fraction of primate genomes. They contribute to genetic variation and provide raw material for evolution. Groups of SDs are characterized by the presence of shared core duplicons. One of these core duplicons, low copy repeat (lcr)16a, has been shown to be particularly active in the propagation of interspersed SDs in primates. The underlying mechanisms are, however, only partially understood. Alu short interspersed elements (SINEs) are frequently found at breakpoints and have been implicated in the expansion of SDs.Detailed analysis of lcr16a-containing SDs shows that the hominid-specific SVA (SINE-R-VNTR-Alu) retrotransposon is an integral component of the core duplicon in Asian and African great apes. In orang-utan, it provides breakpoints and contributes to both interchromosomal and intrachromosomal lcr16a mobility by inter-element recombination. Furthermore, the data suggest that in hominines (human, chimpanzee, gorilla) SVA recombination-mediated integration of a circular intermediate is the founding event of a lineage-specific lcr16a expansion. One of the hominine lcr16a copies displays large flanking direct repeats, a structural feature shared by other SDs in the human genome.Taken together, the results obtained extend the range of SVAs’ contribution to genome evolution from RNA-mediated transduction to DNA-based recombination. In addition, they provide further support for a role of circular intermediates in SD mobilization.     

Lateral gene transfer between prokaryotes and multicellular eukaryotes: ongoing and significant?

The expansion of genome sequencing projects has produced accumulating evidence for lateral transfer of genes between prokaryotic and eukaryotic genomes. However, it remains controversial whether these genes are of functional importance in their recipient host. Nikoh and Nakabachi, in a recent paper in BMC Biology, take a first step and show that two genes of bacterial origin are highly expressed in the pea aphid Acyrthosiphon pisum. Active gene expression of transferred genes is supported by three other recent studies. Future studies should reveal whether functional proteins are produced and whether and how these are targeted to the appropriate compartment. We argue that the transfer of genes between host and symbiont may occasionally be of great evolutionary importance, particularly in the evolution of the symbiotic interaction itself.     

Interkingdom protein domain fusion: the case of an antimicrobial protein in potato (Solanum tuberosum)

Horizontal gene transfer (HGT) is thought to have been involved in both prokaryotic and eukaryotic evolution. However, the extent to which it shapes eukaryotic genomes is still questionable. The ability to detect and study horizontal gene transfer events is of significant importance to our understanding of its effect on the evolution of eukaryotic genes and genomes. We performed phylogenetic analysis of a published anti-bacterial protein AP1 from potato (Solanum tuberosum). One domain encodes a phosphoesterase with high similarity to an acid phosphatase of Ralstonia solanacearum and closely related Betaproteobacteria. The second domain encodes an UspA-like domain similar to those present in plants. Our phylogenetic analyses suggest that both domains evolved along different evolutionary pathways until they merged into a single gene. We propose that the phosphoesterase domain was acquired by HGT. Our results support claims in favor of HGT detection at the protein domain level. The case of anti-bacterial protein AP1 in potato highlights the significance of gene fusion/protein domain fusion as an important feature of horizontal gene transfer which may contribute substantially to the adaptive abilities of eukaryotic organisms.     

Insertion of Horizontally Transferred Genes within Conserved Syntenic Regions of Yeast Genomes

Horizontal gene transfer has been occasionally mentioned in eukaryotic genomes, but such events appear much less numerous than in prokaryotes, where they play important functional and evolutionary roles. In yeasts, few independent cases have been described, some of which corresponding to major metabolic functions, but no systematic screening of horizontally transferred genes has been attempted so far. Taking advantage of the synteny conservation among five newly sequenced and annotated genomes of Saccharomycetaceae, we carried out a systematic search for HGT candidates amidst genes present in only one species within conserved synteny blocks. Out of 255 species-specific genes, we discovered 11 candidates for HGT, based on their similarity with bacterial proteins and on reconstructed phylogenies. This corresponds to a minimum of six transfer events because some horizontally acquired genes appear to rapidly duplicate in yeast genomes (e.g. YwqG genes in Kluyveromyces thermotolerans and serine recombinase genes of the IS607 family in Saccharomyces kluyveri). We show that the resulting copies are submitted to a strong functional selective pressure. The mechanisms of DNA transfer and integration are discussed, in relation with the generally small size of HGT candidates. Our results on a limited set of species expand by 50% the number of previously published HGT cases in hemiascomycetous yeasts, suggesting that this type of event is more frequent than usually thought. Our restrictive method does not exclude the possibility that additional HGT events exist. Actually, ancestral events common to several yeast species must have been overlooked, and the absence of homologs in present databases leaves open the question of the origin of the 244 remaining species-specific genes inserted within conserved synteny blocks.     

Aldehyde dehydrogenase gene superfamily: the 2000 update

Aldehyde dehydrogenase (ALDH) superfamily represents a group of NAD(P)⁺-dependent enzymes that catalyze the oxidation of a wide spectrum of endogenous and exogenous aldehydes. With the advent of megabase genome sequencing, the ALDH superfamily is expanding rapidly on many fronts. As expected, ALDH genes are found in virtually all genomes analyzed to date, indicating the importance of these enzymes in biological functions. Complete genome sequences of various species have revealed additional ALDH genes. As of July 2000, the ALDH superfamily consists of 331 distinct genes, of which eight are found in archaea, 165 in eubacteria, and 158 in eukaryota. The number of ALDH genes in some species with their genomes completely sequenced and annotated, Escherichia coli and Caenorhabditis elegans, ranges from 10 to 17. In the human genome, 17 functional genes and three pseudogenes have been identified to date. Divergent evolution, based on multiple alignment analysis of 86 eukaryotic ALDH amino-acid sequences, was the basis of the standardized ALDH gene nomenclature system (Pharmacogenetics 9: 421–434, 1999). Thus far, the eukaryotic ALDHs comprise 20 gene families. A complete list of all ALDH sequences known to date is presented here along with the evolution analysis of the eukaryotic ALDHs.     

New names for old strains? <Emphasis Type="Italic">Wolbachia w</Emphasis>Sim is actually <Emphasis Type="Italic">w</Emphasis>Ri

A response to Serendipitous discovery of Wolbachia genomes in multiple Drosophila species by SL Salzberg, JC Dunning Hotopp, AL Delcher, M Pop, DR Smith, MB Eisen and WC Nelson. Genome Biology 2005, 6:R23     

Genomic diversity of the human intestinal parasite Entamoeba histolytica

Background

Entamoeba histolytica is a significant cause of disease worldwide. However, little is known about the genetic diversity of the parasite. We re-sequenced the genomes of ten laboratory cultured lines of the eukaryotic pathogen Entamoeba histolytica in order to develop a picture of genetic diversity across the genome.

Results

The extreme nucleotide composition bias and repetitiveness of the E. histolytica genome provide a challenge for short-read mapping, yet we were able to define putative single nucleotide polymorphisms in a large portion of the genome. The results suggest a rather low level of single nucleotide diversity, although genes and gene families with putative roles in virulence are among the more polymorphic genes. We did observe large differences in coverage depth among genes, indicating differences in gene copy number between genomes. We found evidence indicating that recombination has occurred in the history of the sequenced genomes, suggesting that E. histolytica may reproduce sexually.

Conclusions

E. histolytica displays a relatively low level of nucleotide diversity across its genome. However, large differences in gene family content and gene copy number are seen among the sequenced genomes. The pattern of polymorphism indicates that E. histolytica reproduces sexually, or has done so in the past, which has previously been suggested but not proven.     

A comprehensive evolutionary classification of proteins encoded in complete eukaryotic genomes

Background

Sequencing the genomes of multiple, taxonomically diverse eukaryotes enables in-depth comparative-genomic analysis which is expected to help in reconstructing ancestral eukaryotic genomes and major events in eukaryotic evolution and in making functional predictions for currently uncharacterized conserved genes.

Results

We examined functional and evolutionary patterns in the recently constructed set of 5,873 clusters of predicted orthologs (eukaryotic orthologous groups or KOGs) from seven eukaryotic genomes: Caenorhabditis elegans, Drosophila melanogaster, Homo sapiens, Arabidopsis thaliana, Saccharomyces cerevisiae, Schizosaccharomyces pombe and Encephalitozoon cuniculi. Conservation of KOGs through the phyletic range of eukaryotes strongly correlates with their functions and with the effect of gene knockout on the organism's viability. The approximately 40% of KOGs that are represented in six or seven species are enriched in proteins responsible for housekeeping functions, particularly translation and RNA processing. These conserved KOGs are often essential for survival and might approximate the minimal set of essential eukaryotic genes. The 131 single-member, pan-eukaryotic KOGs we identified were examined in detail. For around 20 that remained uncharacterized, functions were predicted by in-depth sequence analysis and examination of genomic context. Nearly all these proteins are subunits of known or predicted multiprotein complexes, in agreement with the balance hypothesis of evolution of gene copy number. Other KOGs show a variety of phyletic patterns, which points to major contributions of lineage-specific gene loss and the 'invention' of genes new to eukaryotic evolution. Examination of the sets of KOGs lost in individual lineages reveals co-elimination of functionally connected genes. Parsimonious scenarios of eukaryotic genome evolution and gene sets for ancestral eukaryotic forms were reconstructed. The gene set of the last common ancestor of the crown group consists of 3,413 KOGs and largely includes proteins involved in genome replication and expression, and central metabolism. Only 44% of the KOGs, mostly from the reconstructed gene set of the last common ancestor of the crown group, have detectable homologs in prokaryotes; the remainder apparently evolved via duplication with divergence and invention of new genes.

Conclusions

The KOG analysis reveals a conserved core of largely essential eukaryotic genes as well as major diversification and innovation associated with evolution of eukaryotic genomes. The results provide quantitative support for major trends of eukaryotic evolution noticed previously at the qualitative level and a basis for detailed reconstruction of evolution of eukaryotic genomes and biology of ancestral forms.