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Rainbow Trout Genome Gives Look into Consequences of Genome Duplications

NEW YORK (GenomeWeb) – By sequencing the rainbow trout genome, an international team of researchers led by Yann Guiguen at the French National Institutes for Agricultural Research has been able to peek into the changes that occur after a whole-genome duplication event.

While whole-genome duplications events mark important evolutionary events in vertebrate lineages, they are both rare and ancient occurrences. But within the salmonid lineage, which includes the rainbow trout Oncorhynchus mykiss, there was a relatively recent duplication event that took place some 25 million to 100 million years ago.

As the researchers reported in Nature Communications today, the rainbow trout genome indicates that, after duplication, there has been an ongoing slow and step-wise return to a diploid genome rather than a rapid and large-scale reorganization, challenging previous findings.

In the past 100 million years or so since the duplication, the rainbow trout genome has lost about half of the duplicated protein-coding genes, but retained nearly all of its duplicated microRNA genes, the researchers added.

"In humans and most vertebrates the duplication events were older so there are fewer duplicated genes still present," Gary Thorgaard, a co-author from Washington State University, said in a statement. "Most of the duplicated genes get lost or modified so much that they are no longer recognizable as duplicates over time. In the trout and salmon, we can see an earlier stage in the process and many duplicated genes are still present."

The team sequenced a male rainbow trout from the Alaskan Swanson River clonal line using both 454 and Illumina sequencing platforms. The assembly includes 46,585 annotated protein-coding genes.

The researchers reconstructed the double-conserved synteny, or paralogous regions originating from the salmonid-specific duplication event. They then compared what they generated to non-salmonid teleost fish genomes.

Overall, the trout genome harbors 38 pairs of large duplicated regions that are spread over its 30 chromosomes. Fourteen of those regions correspond to the fusion of two different post-salmonid-specific doubling event chromosomes, while other chromosomes are mosaics.

Within the double-conserved synteny regions, the researchers found some 6,733 ohnologs, or paralogs formed by a doubling event. By calculating the distribution of silent substitutions in these ohnolog pairs as well as in Atlantic salmon and rainbow trout paralog pairs, the team traced the doubling event back to about 96 million years ago.

Since that event some 96 million years ago, the researchers found that the two ancestral genome copies have remained fairly stable — just more than half of the duplicated genes have undergone gene fractionation and returned to a single-copy state.

They also estimated that the pre-doubling genome included 31,476 genes, of which 16,368 genes have been retained as single copies. That, they noted, corresponds to an average gene inactivation rate of about 170 genes per million years since the salmonid-specific doubling event.

The researchers also found instances of pseudogenization events and noted that these pseudogenes have low sequence divergence as compared to the corresponding functional copy.

"Altogether these multiple evidences suggest that gene fractionation is a slow process, largely incomplete and still in progress in the trout genome," Guiguen and his colleagues said. "This challenges the current hypothesis that [whole-genome duplication events] are followed by massive and rapid genomic reorganizations and gene deletions."

Additionally, the researchers found that microRNA genes are even more highly conserved. Some 97 percent, or 233 of the 241 miRNA loci, in the double-conserved synteny region are present as duplicated copies.

"It is, however, noteworthy that miRNAs are acting in a dose-dependent manner to tune gene expression at post-transcriptional level and that miRNAs have several, if not many, targets among protein-coding mRNAs," the researchers added. "It is thus possible that all duplicated copies of miRNA genes are still necessary to control gene expression in the context of a recent [whole genome duplication event]."

Prior to this doubling event, the lineage leading up to salmonids underwent other, more ancient duplications. For instance, the teleost-specific doubling event is pegged to have occurred about 225 million to 333 million years ago.

Some genes, Guiguen and his colleagues found, seem to be preferentially kept as duplicates in that and older doublings. A gene ontology analysis indicated an enrichment of ohnologs from these ancient events involved in processes such as embryonic and neuronal development. Analysis of the more recent salmonid-specific ohnologs didn't yield significant results, possibly, the researchers said, because gene fractionation is still ongoing.

Still, a number of ohnologs from the salmonid-specific doubling showed differences in their expression profiles and expression levels in the 15 tissues the researchers analyzed.

"Following [doubling], it is well accepted that the remaining ohnologs can acquire new expression patterns potentially leading to neo- or subfunctionalization," Guiguen and colleagues added. "This suggests that evolution after WGD is also acting on regulatory regions of these ohnologous genes that could subsequently be either silenced, or sub- or neo-functionalized."