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Tetraploid African Clawed Frog Genome Shows Unequal Evolution

NEW YORK (GenomeWeb) – A US- and Japan-led team of researchers has sequenced the genome of the tetraploid African clawed frog, Xenopus laevis.

Because it contains four pairs of chromosomes rather than the two pairs that diploid genomes have, the researchers combined two methods — whole-genome shotgun sequencing and long-insert clone-based end sequencing — to assemble the X. laevis genome. As they reported in Nature this week, the researchers compared that assembly to that of the related, but diploid, Western clawed frog X. tropicalis genome to determine when the allotetraploid event occurred and how the X. laevis genome has been evolving since.

While Xenopus has been tricky to study using genomic tools, it "has become a major vertebrate model supporting cellular and developmental biology research," author Jeremy Schmutz from the HudsonAlpha Institute for Biotechnology noted in a statement.

In particular, the researchers sequenced an inbred X. laevis strain using a whole- genome shotgun approach and a long-insert clone-based end sequencing approach. They organized those reads into chromosomes by using both fluorescence in situ hybridization of some 800 bacterial artificial chromosome clones and chromatin conformation capture analysis.

The combination of these approaches enabled the investigators to develop a draft of the X. laevis genome that assigned 90 percent of predicted protein-coding genes to a chromosomal location. In addition, they annotated more than 45,000 protein-coding genes and 342 microRNAs using RNA-seq data from 14 tissues.

A karyotype of X. laevis showed nine pairs of homologous chromosomes, one set of which was generally smaller than the other set. And the researchers found they could place some 24,000 protein-coding genes into two-to-one or one-to-one correspondence with X. tropicalis genes.

Using transposable elements as markers, the investigators traced back the progenitors of the X. laevis subgenomes. They reported that L and S chromosome sets — L and S for 'long' and 'short' — are the descendants of two distinct diploid progenitors.

"[W]e could find distinct transposable element relicts that proved the whole­genome duplication to be the result of two extinct progenitor species," author Adam Session from the Department of Energy Joint Genome Institute said in a statement. "While this has been shown in many grasses, this is the first time this has been experimentally shown without extant progenitors."

In addition, he and his colleagues estimated that the subgenomes diverged from one another 34 million years ago, and from X. tropicalis 48 million years ago. They further estimated that the allotetraploid event occurred between 17 million years and 18 million years ago, noting that the timing broadly corresponds with other estimates of tetraploid Xenopus radiation.

The X. laevis and X. tropicalis chromosomes have largely retained synteny, and the X. laevis L subgenome and X. tropicalis also exhibit collinearity, the researchers said. This indicates that they represent the ancestral chromosomal state. The S subgenome, meanwhile, has undergone intrachromosomal rearrangements and deletions.

Still, 56 percent of the duplicated protein-coding genes within X. laevis have been kept, according to the researchers. Certain types of genes were more likely to be kept or lost — for instance, DNA binding protein genes as well as genes involved in developmentally regulated signaling and cell cycle regulation pathways were kept at a higher rate, while genes involved in DNA repair and metabolic genes were more likely to be lost.

At the same time, the researchers uncovered shifts in gene expression between retained homologous gene pairs. Genes from the L subgenome were typically expressed at a higher rate in adult tissues than the copy from the S subgenome, but other times the two genes were differentially expressed.

All this, the researchers noted, suggests that the X. laevis subgenomes have been evolving asymmetrically.

In an accompanying commentary in Nature, the National Human Genome Research Institute's Shawn Burgess said that the X. laevis genome will provide a resource for researchers.

"Developmental biologists now have at their disposal the detailed genomic information so essential to modern biology," Burgess wrote. "Genome biologists have proof that even large, complex genome duplications can ultimately be resolved into high-quality assemblies."

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