Degenerate Tetraploidy Was Established Before Bdelloid Rotifer Families Diverged

Hur, Jae H.; Doninck, Karine Van; Mandigo, Morgan; Meselson, Matthew

doi:10.1093/molbev/msn260

Cited by 59 publications

(88 citation statements)

References 37 publications

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“…The A. vaga rvt did not fall into any of the known RT categories, such as retrons, retroplasmids, group II introns, telomerases, non-LTR retrotransposons, LTR retrotransposons, retroviruses, and pararetroviruses. Its single-copy status was established by Southern blot hybridization of genomic DNA and by exhaustive screening of the A. vaga genomic library (17). In this library, we found a colinear pair of rvt-containing fosmids with 4% overall divergence, consistent with the genome structure of bdelloid rotifers in which chromosomes occur as colinear allelic pairs with overall divergence up to 6% (17,18).…”

Section: Resultssupporting

confidence: 57%

“…Its single-copy status was established by Southern blot hybridization of genomic DNA and by exhaustive screening of the A. vaga genomic library (17). In this library, we found a colinear pair of rvt-containing fosmids with 4% overall divergence, consistent with the genome structure of bdelloid rotifers in which chromosomes occur as colinear allelic pairs with overall divergence up to 6% (17,18). The divergence between members of the rvt pair is <1%, either at the nucleotide level (13/2,490 nt substitutions) or at the protein level (6/829 aa substitutions).…”

Section: Resultssupporting

confidence: 57%

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A widespread class of reverse transcriptase-related cellular genes

Gladyshev

Arkhipova

2011

Proc. Natl. Acad. Sci. U.S.A.

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Reverse transcriptases (RTs) polymerize DNA on RNA templates. They fall into several structurally related but distinct classes and form an assemblage of RT-like enzymes that, in addition to RTs, also includes certain viral RNA-dependent RNA polymerases (RdRP) synthesizing RNA on RNA templates. It is generally believed that most RT-like enzymes originate from retrotransposons or viruses and have no specific function in the host cell, with telomerases being the only notable exception. Here we report on the discovery and properties of a unique class of RT-related cellular genes collectively named rvt. We present evidence that rvts are not components of retrotransposons or viruses, but single-copy genes with a characteristic domain structure that may contain introns in evolutionarily conserved positions, occur in syntenic regions, and evolve under purifying selection. These genes can be found in all major taxonomic groups including protists, fungi, animals, plants, and even bacteria, although they exhibit patchy phylogenetic distribution in each kingdom. We also show that the RVT protein purified from one of its natural hosts, Neurospora crassa, exists in a multimeric form and has the ability to polymerize NTPs as well as dNTPs in vitro, with a strong preference for NTPs, using Mn 2+ as a cofactor. The existence of a previously unknown class of single-copy RT-related genes calls for reevaluation of the current views on evolution and functional roles of RNA-dependent polymerases in living cells.D NA-dependent polymerases are essential for cellular function, as they mediate the flow of genetic information from DNA to RNA to proteins (1). In contrast, RNA-dependent polymerases have long been associated with replication of selfish and parasitic genetic elements, such as viruses or transposons. Although the discovery of reverse transcriptase (RT) challenged the concept of unidirectionality of the flow of genetic information, this reverse direction has been reserved for retroviruses, pararetroviruses (hepadna-and caulimoviruses), and other RT-containing multicopy entities such as non-LTR and LTR retrotransposons, group II introns, retrons, and retroplasmids, as well as occasional retro (pseudo)genes (2-4). Similarly, viral RNA-dependent RNA polymerases (RdRPs), enzymes structurally related to RTs, serve to replicate the genomes of viruses that use RNA as genetic material (5). These and certain other polymerases are unified by the architecture known as "right hand," composed of the three subdomains called fingers, palm, and thumb (6). Like all polymerases, they use two-metal-ion catalysis for phosphoryl transfer reactions resulting in nucleotide addition.In 1997, this diverse superfamily of enzymes was joined by the telomerase reverse transcriptase (TERT), a specialized RT that maintains the ends of eukaryotic linear chromosomes by addition of short G-rich repeated DNA sequences that are copied multiple times via reverse transcription of a specific region of the associated RNA template constituting part of the holoenzyme (...

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Section: Resultssupporting

confidence: 57%

Section: Resultssupporting

confidence: 57%

A widespread class of reverse transcriptase-related cellular genes

Gladyshev

Arkhipova

2011

Proc. Natl. Acad. Sci. U.S.A.

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“…Recent reports suggest that the asexual bdelloid rotifers are tetraploid (Mark Welch et al 2008) and that gene conversion occurs between gene copies (Hur et al 2008;Mark Welch et al 2008). Our model supports the verbal claim that gene conversion between homologous gene copies might aid in DNA damage repair and prevent the genomic degradation that is expected to accompany strict asexual reproduction.…”

Section: Discussionmentioning

confidence: 99%

Gene Duplication, Gene Conversion and the Evolution of the Y Chromosome

Connallon

Clark

2010

Genetics

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Nonrecombining chromosomes, such as the Y, are expected to degenerate over time due to reduced efficacy of natural selection compared to chromosomes that recombine. However, gene duplication, coupled with gene conversion between duplicate pairs, can potentially counteract forces of evolutionary decay that accompany asexual reproduction. Using a combination of analytical and computer simulation methods, we explicitly show that, although gene conversion has little impact on the probability that duplicates become fixed within a population, conversion can be effective at maintaining the functionality of Y-linked duplicates that have already become fixed. The coupling of Y-linked gene duplication and gene conversion between paralogs can also prove costly by increasing the rate of nonhomologous crossovers between duplicate pairs. Such crossovers can generate an abnormal Y chromosome, as was recently shown to reduce male fertility in humans. The results represent a step toward explaining some of the more peculiar attributes of the human Y as well as preliminary Y-linked sequence data from other mammals and Drosophila. The results may also be applicable to the recently observed pattern of tetraploidy and gene conversion in asexual, bdelloid rotifers.

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“…More than 20% of genes with AI . 45 are found in quartets (groups of four homologous copies in conserved syntenic regions) and were therefore probably incorporated into the rotifer genome before the establishment of tetraploidy, which itself pre-dates the divergence of extant bdelloid families 8 . The higher the number of copies of a putative HGT gene, the higher its number of introns and the closer its guanine-cytosine (GC) content to the A. vaga genome average ( Supplementary Fig.…”

Section: Research Lettermentioning

confidence: 99%

“…Allelic pairs of coding sequences are on average 96.2% identical at the nucleotide level (median 5 98.6%) versus 73.6% (median 5 75.1%) for ohnologous pairs. Nearly 40% (84.5 Mb) of the assembled genome sequence is organized in quartets of four homologous regions A 1 , A 2 , B 1 and B 2 , of which A 1 -A 2 and B 1 -B 2 are two pairs of alleles and As are ohnologous to Bs 8 (Fig. 2b).…”

mentioning

confidence: 99%

Genomic evidence for ameiotic evolution in the bdelloid rotifer Adineta vaga

Flot

Hespeels

et al. 2013

Nature

363

624

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Loss of sexual reproduction is considered an evolutionary dead end for metazoans, but bdelloid rotifers challenge this view as they appear to have persisted asexually for millions of years 1 . Neither male sex organs nor meiosis have ever been observed in these microscopic animals: oocytes are formed through mitotic divisions, with no reduction of chromosome number and no indication of chromosome pairing 2 . However, current evidence does not exclude that they may engage in sex on rare, cryptic occasions. Here we report the genome of a bdelloid rotifer, Adineta vaga (Davis, 1873) 3 , and show that its structure is incompatible with conventional meiosis. At gene scale, the genome of A. vaga is tetraploid and comprises both anciently duplicated segments and less divergent allelic regions. However, in contrast to sexual species, the allelic regions are rearranged and sometimes even found on the same chromosome. Such structure does not allow meiotic pairing; instead, we find abundant evidence of gene conversion, which may limit the accumulation of deleterious mutations in the absence of meiosis. Gene families involved in resistance to oxidation, carbohydrate metabolism and defence against transposons are significantly expanded, which may explain why transposable elements cover only 3% of the assembled sequence. Furthermore, 8% of the genes are likely to be of non-metazoan origin and were probably acquired horizontally. This apparent convergence between bdelloids and prokaryotes sheds new light on the evolutionary significance of sex.With more than 460 described species 4 , bdelloid rotifers ( Fig. 1) represent the highest metazoan taxonomic rank in which males, hermaphrodites and meiosis are unknown. Such persistence and diversification of an ameiotic clade of animals are in contradiction with the supposed long-term disadvantages of asexuality, making bdelloids an 'evolutionary scandal' 5 . Another unusual feature of bdelloid rotifers is their extreme resistance to desiccation at any stage of their life cycle 6 , enabling these microscopic animals to dwell in ephemeral freshwater habitats such as mosses, lichens and forest litter; this ability is presumably the source of their extreme resistance to ionizing radiation 7 .We assembled the genome of a clonal A. vaga lineage into separate haplotypes with a N 50 of 260 kilobases (kb) (that is, half of the assembly was composed of fragments longer than 260 kb). Assembly size was 218 megabases (Mb) but 26 Mb of the sequence had twice the average sequencing coverage, suggesting that some nearly identical regions were not resolved during assembly ( Supplementary Fig. 3); hence, the total genome size is likely to be 244 Mb, which corresponds to the estimate obtained independently using fluorometry (Supplementary Note C2). Annotation of the complete assembly (including all haplotypes) yielded 49,300 genes. Intragenomic sequence comparisons revealed numerous homologous blocks with conserved gene order (colinear regions). For each such block we computed the per-site synonymous d...

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Degenerate Tetraploidy Was Established Before Bdelloid Rotifer Families Diverged

Cited by 59 publications

References 37 publications

A widespread class of reverse transcriptase-related cellular genes

A widespread class of reverse transcriptase-related cellular genes

Gene Duplication, Gene Conversion and the Evolution of the Y Chromosome

Genomic evidence for ameiotic evolution in the bdelloid rotifer Adineta vaga

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