Evolutionary genomics of chromoviruses in eukaryotes

The diversity, origin, and evolution of chromoviruses in Eukaryota were examined using the massive amount of genome sequence data for different eukaryotic lineages. A surprisingly large number of novel full-length chromoviral elements were found, greatly exceeding the number of the known chromoviruses. These new elements are mostly structurally intact and highly conserved. Chromoviruses in the key Amniota lineage, the reptiles, have been analyzed by PCR to explain their evolutionary dynamics in amniotes. Phylogenetic analyses provide evidence for a novel centromere-specific chromoviral clade that is widespread and highly conserved in all seed plants. Chromoviral diversity in plants, fungi, and vertebrates, as shown by phylogenetic analyses, was found to be much greater than previously expected. The age of plant chromoviruses has been significantly extended by finding their representatives in the most basal plant lineages, the green and the red algae. The evolutionary origin of chromoviruses has been found to be no earlier than in Cercozoa. The evolutionary history and dynamics of chromoviruses can be explained simply by strict vertical transmission in plants, followed by more complex evolution in fungi and in Metazoa. The currently available data clearly show that chromoviruses indeed represent the oldest and the most widespread clade of Metaviridae.     

Phylogenomic analysis of chromoviruses

Genome sequences of model organisms provide a unique opportunity to obtain insight into the complete diversity of any transposable element (TE) group. A limited number of chromoviruses, the chromodomain containing genus of Metaviridae, is known from plant, fungal and vertebrate genomes. By searching diverse eukaryotic genome databases, we have found a surprisingly large number of new, structurally intact and highly conserved chromoviral elements, greatly exceeding the number of previously known chromoviruses. In this study, we examined the diversity, origin and evolution of chromoviruses in Eukaryota. Chromoviral diversity in plants, fungi and vertebrates, as shown by phylogenetic analyses, was found to be much greater than previously expected. A novel centromere-specific chromoviral lineage was found to be widespread and highly conserved in all seed plants. The age of chromoviruses has been significantly extended by finding their representatives in the most basal plant lineages (green and red algae), in Heterokonta (oomycetes) and in Cercozoa (plasmodiophorids). The evolutionary origin of chromoviruses has been found to be no earlier than in Cercozoa, since none can be found in the basal eukaryotic lineages, despite the extensive genome data. The evolutionary dynamics of chromoviruses can be explained by a strict vertical transmission in plants and fungi, while in Metazoa it is more complex. The currently available genome data clearly show that chromoviruses are the most widespread and one of the oldest Metaviridae clade.     

Characterization of the LTR retrotransposon repertoire of a plant clade of six diploid and one tetraploid species

Comparisons of closely related species are needed to understand the fine‐scale dynamics of retrotransposon evolution in flowering plants. Towards this goal, we classified the long terminal repeat (LTR) retrotransposons from six diploid and one tetraploid species of Orobanchaceae. The study species are the autotrophic, non‐parasitic Lindenbergia philippensis (as an out‐group) and six closely related holoparasitic species of Orobanche [O. crenata, O. cumana, O. gracilis (tetraploid) and O. pancicii] and Phelipanche (P. lavandulacea and P. ramosa). All major plant LTR retrotransposon clades could be identified, and appear to be inherited from a common ancestor. Species of Orobanche, but not Phelipanche, are enriched in Ty3/Gypsy retrotransposons due to a diversification of elements, especially chromoviruses. This is particularly striking in O. gracilis, where tetraploidization seems to have contributed to the Ty3/Gypsy enrichment and led to the emergence of seven large species‐specific families of chromoviruses. The preferential insertion of chromoviruses in heterochromatin via their chromodomains might have favored their diversification and enrichment. Our phylogenetic analyses of LTR retrotransposons from Orobanchaceae also revealed that the Bianca clade of Ty1/Copia and the SMART‐related elements are much more widely distributed among angiosperms than previously known.     

The sunflower (Helianthus annuus L.) genome reflects a recent history of biased accumulation of transposable elements

Aside from polyploidy, transposable elements are the major drivers of genome size increases in plants. Thus, understanding the diversity and evolutionary dynamics of transposable elements in sunflower (Helianthus annuus L.), especially given its large genome size (～3.5 Gb) and the well‐documented cases of amplification of certain transposons within the genus, is of considerable importance for understanding the evolutionary history of this emerging model species. By analyzing approximately 25% of the sunflower genome from random sequence reads and assembled bacterial artificial chromosome (BAC) clones, we show that it is composed of over 81% transposable elements, 77% of which are long terminal repeat (LTR) retrotransposons. Moreover, the LTR retrotransposon fraction in BAC clones harboring genes is disproportionately composed of chromodomain‐containing Gypsy LTR retrotransposons (‘chromoviruses’), and the majority of the intact chromoviruses contain tandem chromodomain duplications. We show that there is a bias in the efficacy of homologous recombination in removing LTR retrotransposon DNA, thereby providing insight into the mechanisms associated with transposable element (TE) composition in the sunflower genome. We also show that the vast majority of observed LTR retrotransposon insertions have likely occurred since the origin of this species, providing further evidence that biased LTR retrotransposon activity has played a major role in shaping the chromatin and DNA landscape of the sunflower genome. Although our findings on LTR retrotransposon age and structure could be influenced by the selection of the BAC clones analyzed, a global analysis of random sequence reads indicates that the evolutionary patterns described herein apply to the sunflower genome as a whole.     

Diversity and evolution of LTR retrotransposons in the genome of <Emphasis Type="Italic">Phanerochaete chrysosporium</Emphasis> (Fungi: Basidiomycota)

The diversity of mobile elements, in particular LTR retrotransposons, in basidiomycetes fungi has been poorly studied. The genome of the lignin-degrading fungus Phanerochaete chrysosporium was screened for LTR retrotransposons. A surprisingly high diversity of LTR retrotransposons was found. Twenty-three novel mobile elements from two superfamilies, Pseudoviridae and Metaviridae, were described. The proportion of LTR retrotransposons in the P. chrysosporium genome is low, constituting only about 3%. Nevertheless, LTR retrotransposons of P. chrysosporium represent a dynamic part of the genome, which is evidenced by the presence of intact copies with signs of recent transposition and numerous solo LTR elements. Phylogenetic and structural analyses detected mobile elements having characteristics that had been previously unknown for other LTR retrotransposons.     

Comparative genomics in the Amoebozoa clade

Amoeboid life forms can be found throughout the evolutionary tree. The greatest proportion of these life forms is found in the Amoebozoa clade, one of the six major eukaryote evolutionary branches. Despite its common origin this clade exhibits a wide diversity of lifestyles including free‐living and parasitic species and species with multicellular and multinucleate life stages. In this group, development, cooperation, and social behaviour can be studied in addition to traits common to unicellular organisms. To date, only a few Amoebozoa genomes have been sequenced completely, however a number of expressed sequence tags (ESTs) and complete and draft genomes have become available recently for several species that represent some of the major evolutionary lineages in this clade. This resource allows us to compare and analyse the evolutionary history and fate of branch‐specific genes if properly exploited. Despite the large evolutionary time scale since the emergence of the major groups the genomic organization in Amoebozoa has retained common features. The number of Amoebozoa‐specific genetic inventions seems to be rather small. The emergence of subgroups is accompanied by gene and domain losses and acquisitions of bacterial gene material. The sophisticated developmental cycles of Myxogastria and Dictyosteliida likely have a common origin and are deeply rooted in amoebozoan evolution. In this review we describe initial approaches to comparative genomics in Amoebozoa, summarize recent findings, and identify goals for further studies.     

Evolutionary dynamics of an ancient retrotransposon family provides insights into evolution of genome size in the genus Oryza

Long terminal repeat (LTR) retrotransposons constitute a significant portion of most eukaryote genomes and can dramatically change genome size and organization. Although LTR retrotransposon content variation is well documented, the dynamics of genomic flux caused by their activity are poorly understood on an evolutionary time scale. This is primarily because of the lack of an experimental system composed of closely related species whose divergence times are within the limits of the ability to detect ancestrally related retrotransposons. The genus Oryza, with 24 species, ten genome types, different ploidy levels and over threefold genome size variation, constitutes an ideal experimental system to explore genus-level transposon dynamics. Here we present data on the discovery and characterization of an LTR retrotransposon family named RWG in the genus Oryza. Comparative analysis of transposon content (approximately 20 to 27,000 copies) and transpositional history of this family across the genus revealed a broad spectrum of independent and lineage-specific changes that have implications for the evolution of genome size and organization. In particular, we provide evidence that the basal GG genome of Oryza (O. granulata) has expanded by nearly 25% by a burst of the RWG lineage Gran3 subsequent to speciation. Finally we describe the recent evolutionary origin of Dasheng, a large retrotransposon derivative of the RWG family, specifically found in the A, B and C genome lineages of Oryza.     

Evolution of target specificity in R1 clade non-LTR retrotransposons

Although most non-long terminal repeat (non-LTR) retrotransposons are inserted throughout the host genome, many non-LTR elements in the R1 clade are inserted into specific sites within the target sequence. Four R1 clade families have distinct target specificity: R1 and RT insert into specific sites of 28S rDNA, and TRAS and SART insert into different sites within the (TTAGG)(n) telomeric repeats. To study the evolutionary history of target specificity of R1-clade retrotransposons, we have screened extensively novel representatives of the clade from various insects by in silico and degenerate polymerase chain reaction (PCR) cloning. We found four novel sequence-specific elements; Waldo (WaldoAg1, 2, and WaldoFs1) inserts into ACAY repeats, Mino (MinoAg1) into AC repeats, R6 into another specific site of the 28S rDNA, and R7 into a specific site of the 18S rDNA. In contrast, several elements (HOPE, WISHBm1, HidaAg1, NotoAg1, KagaAg1, Ha1Fs1) lost target sequence specificity, although some of them have preferred target sequences. Phylogenetic trees based on the RT and EN domains of each element showed that (1) three rDNA-specific elements, RT, R6, and R7, diverged from Waldo; (2) the elements having similar target sequences are phylogenetically related; and (3) the target specificity in the R1 clade was obtained once and thereafter altered and lost several times independently. These data indicate that the target specificity in R1 clade retroelements has changed during evolution and is more divergent than has been speculated so far.     

The Role of Interelement Selection in Saccharomyces cerevisiae Ty Element Evolution

Retrotransposons are mobile genetic elements that are ubiquitous components of eukaryotic genomes. The evolutionary success of retrotransposons is explained by their ability to replicate faster than the host genomes in which they reside. Elements with higher rates of genomic replication possess a selective advantage over less active elements. Retrotransposon populations, therefore, are shaped largely by selective forces acting at the genomic level between elements. To evaluate rigorously the effects of selective forces acting on retrotransposons, detailed information on the patterns of molecular variation within and between retrotransposon families is needed. The sequencing of the Saccharomyces cerevisiae genome, which includes the entire genomic complement of yeast retrotransposons, provides an unprecedented opportunity to access and analyze such data. In this study, we analyzed in detail the patterns of nucleotide variation within the open reading frames of two parental (Ty1 and Ty2) and one hybrid (Ty1/2) family of yeast retrotransposons. The pattern and distribution of nucleotide changes on the phylogenetic reconstructions of the three families of Ty elements reveal evidence of negative selection on both internal and external branches of the Ty phylogenies. These results indicate that most, if not all, Ty elements examined represent active or recently active retrotransposon lineages. We discuss the relevance of these findings with respect to the coevolutionary dynamic operating between genomic element populations and the host organisms in which they reside. Received: 5 November 1998 / Accepted: 17 March 1999     

Evolutionary impact of human Alu repetitive elements

Early studies of human Alu retrotransposons focused on their origin, evolution and biological properties, but current focus is shifting toward the effect of Alu elements on evolution of the human genome. Recent analyses indicate that numerous factors have affected the chromosomal distribution of Alu elements over time, including male-driven insertions, deletions and rapid CpG mutations after their retrotransposition. Unequal crossing over between Alu elements can lead to local mutations or to large segmental duplications responsible for genetic diseases and long-term evolutionary changes. Alu elements can also affect human (primate) evolution by introducing alternative splice sites in existing genes. Studying the Alu family in a human genomic context is likely to have general significance for our understanding of the evolutionary impact of other repetitive elements in diverse eukaryotic genomes.     

Proliferation of Ty3/gypsy-like retrotransposons in hybrid sunflower taxa inferred from phylogenetic data

Background  

Long terminal repeat (LTR) retrotransposons are a class of mobile genetic element capable of autonomous transposition via an RNA intermediate. Their large size and proliferative ability make them important contributors to genome size evolution, especially in plants, where they can reach exceptionally high copy numbers and contribute substantially to variation in genome size even among closely related taxa. Using a phylogenetic approach, we characterize dynamics of proliferation events of Ty3/gypsy-like LTR retrotransposons that led to massive genomic expansion in three Helianthus (sunflower) species of ancient hybrid origin. The three hybrid species are independently derived from the same two parental species, offering a unique opportunity to explore patterns of retrotransposon proliferation in light of reticulate evolutionary events in this species group.     

Retroelements: tools for sex chromosome evolution

Many eukaryotic taxa inherit a heteromorphic sex chromosome pair. It is a generally accepted hypothesis that the sex chromosome pair is derived from a pair of homologous autosomes that has developed after the occurrence of a sex differentiator in an evolutionary process into two structurally and functionally different partners. In most of the analyzed systems the occurrence of the dominant sex differentiator is paralleled by the suppression of recombination within and close by that region. The recombinational isolation can spread in an evolutionary selection process from neighboring regions finally over the whole chromosome. Suppression of recombination strongly biases the distribution of retrotransposons in the genome. Our results and that from others indicate that the major force driving the evolution of Y chromosomes are retrotransposons, remodeling euchromatic chromosome structures into heterochromatic ones. In our model, intact or already eroded retrotransposons become trapped due to their inherent transposition mechanisms in non-recombining regions. The massive accumulation of retrotransposons interferes strongly with the activity of genes. We hypothesize that Y chromosome degeneration is a stepwise evolutionary process: (1) Massive accumulation of retrotransposons occurs in the non-recombining regions. (2) Heterochromatic nucleation centers are formed as a consequence of genomic defense against invasive parasitic elements; the established nucleation centers become epigenetically inherited. (3) Spreading of heterochromatin from the nucleation centers into flanking regions induces in an adaptive process gene silencing of neighbored genes that could either be still intact or in an already eroded condition, e.g., showing point mutations, deletions, insertions; the retroelements should be subjects to the same forces of deterioration as the genes themselves. (4) Constitutive silenced genes are not committed to the same genetic selection pressure as active genes and therefore more exposed to the decay process. (5) Gene dosage balance is reestablished by the parallel evolution of dosage compensation mechanisms. The evolving secondary sex chromosomes, neo-X and neo-Y, of Drosophila miranda are revealed to be a unique and potent model system to catch the evolutionary Y deterioration process in progress.     

Two families of non-LTR retrotransposons, Syrinx and Daphne, from the Darwinulid ostracod, Darwinula stevensoni

Two novel families of non-LTR retrotransposons, named Syrinx and Daphne, were cloned and characterized in a putative ancient asexual ostracod Darwinula stevensoni. Phylogenetic analysis reveals that Daphne is the founding member of a novel clade of non-LTR retroelements, which also contains retrotransposon families from the sea urchin and the silkworm and forms a sister clade to L2-like elements. The Syrinx family of non-LTR retrotransposons exhibits evidence of relatively recent activity, manifested in high levels of sequence similarity between individual copies and a three- to ten-fold excess of synonymous substitutions, which is indicative of purifying selection. The Daphne family may have very few copies with intact open reading frames, and exhibits neutral within-family ratio of non-synonymous to synonymous substitutions. It can additionally be characterized by formation of inverted truncated head-to-head structures. All of these features make recent activity less likely than in the Syrinx family. Our results are discussed in light of the evolutionary consequences of long-term asexuality in general and in D. stevensoni in particular.     

Digest: A single genetic origin and a role for bone development pathways in repeated losses of flight in steamer ducks*

Is there evidence for convergence in the molecular mechanisms underlying the loss of flight in the avian evolutionary tree? Campagna et al. used genomic data to investigate the genetic basis of flightlessness in steamer ducks, a recently diverged clade that is polymorphic with respect to flight. They found an association between morphological changes related to flightlessness and several genes, one of which is involved in growth and bone development, providing evidence for a single genetic origin for flightlessness.