How the African clawed frog got an extra pair of genes

October 19, 2016, University of Tokyo
'Fossil' DNA sequences found only in the S subgenome (chromosomes) ofXenopus laevis emit a red glow employing the FISH method. The nine Schromosomes here clearly possess a larger number of red regions, believed tohave derived from ancestral species S. (Chromosome 9, at bottom right, isrepresented as '9_10,' as it corresponds to the fusion of ancestralchromosomes corresponding to chromosomes 9 and 10 in Xenopus tropicalis). Credit: 2016 Yoshinobu Uno.

The African clawed frog's ancestor inherited one set of chromosomes each from two different species and doubled its whole genome some 18 million years ago, according to an international research consortium led by Japanese and American scientists who sequenced the entire genome of the Xenopus laevis for the first time. Scientists hope that the finding will help our understanding of vertebrate evolution, as the vertebrate genome doubled twice 500 million years ago.

X. laevis is unusual in that it is a tetraploid species that has four sets of , while many organisms, including humans, are diploid and have two sets of chromosomes. How and when this came about has been a topic of debate for some time.

One hypothesis is that the tetraploid X. laevis inherited one half of its genetic material from each parent when two diploid ancestral species mated, and the genome of this diploid offspring then doubled, giving rise to a tetraploid organism with twice the number of chromosomes as its ancestors.

"X. laevis is an essential organism for biological and , but the sheer size and complexity of its genome made it difficult for scientists to sequence the genome in its entirety," says Associate Professor Masanori Taira, leader of the Japanese research team at the University of Tokyo. He continues, "He thought that sequencing the entire genome would not only be valuable for biological and biomedical research but also provide clues as to the origins of tetraploidy."

The researchers sequenced the of the J (Japan) strain of the frog inbred in Japan, in which the genetic codes inherited from the mother and father, respectively, are identical.

Though similar in appearance, the tetraploid Xenopus laevis adult female is noticeably larger than its counterpart in the related diploid species Xenopus tropicalis. Credit: 2016 Shuji Takahashi.

The US team led by Dan Rokhsar and Richard Harland at the University of California, Berkeley, used the shotgun method to sequence short fragments of DNA and piece them together like a puzzle. The Japanese team sequenced very long fragments of DNA and determined the location of the long DNA on the chromosomes. This extra step helped to distinguish the separate genome sequences inherited from each ancestral species.

"I thought that analyzing the 'transposable elements' (segments of DNA that move around the genome) that become fixed or inactive over time, might be one way of tracing the two ancestral genomes, present as subgenomes in X. laevis," says Taira.

He suggested this idea to his co-authors, Dr. Akira Hikosaka at Hiroshima University and Dr. Yoshinobu Uno at Nagoya University. They tested Taira's idea and discovered that indeed two sets of chromosomes originated from different diploid ancestors.

Two ancestral species with nine pairs of chromosomes, S and L, mate to produce a hybrid S/L offspring with 18 chromosomes that do not pair. This sterile offspring undergoes whole genome duplication to produce a new fertile species with 18 pairs of chromosomes that is ancestral to all Xenopus species. For clarity, the process is rendered here with only one type of chromosome. Credit: 2016 Masanori Taira.

Curiously, the scientists also found that the subgenomes evolved separately in the nucleus, giving rise to shorter S and longer L types, the first evidence of animal subgenome evolution. The L type chromosomes preserved most of the ancestral genetic information, while the S type showed greater gene loss, deletion and rearrangement.

"Scientists believe that two rounds of whole 500 million years ago contributed to the emergence of the first vertebrate species and an explosion of diversity in this group. We think our discovery will improve our understanding of this important event in our evolutionary history," says Taira.

The genome of the frog X. laevis (top) is roughly double that of its relative, X. tropicalis (bottom). Credit: Professor Atsushi Suzuki, Hiroshima University

Explore further: Scientists unravel genetic ancestry of cultivated strawberry

More information: Adam M. Session et al, Genome evolution in the allotetraploid frog Xenopus laevis, Nature (2016). DOI: 10.1038/nature19840

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