Homoeologous chromosomes of Xenopus laevis are highly conserved after whole-genome duplication

Abstract

It has been suggested that whole-genome duplication (WGD) occurred twice during the evolutionary process of vertebrates around 450 and 500 million years ago, which contributed to an increase in the genomic and phenotypic complexities of vertebrates. However, little is still known about the evolutionary process of homoeologous chromosomes after WGD because many duplicate genes have been lost. Therefore, Xenopus laevis (2n ¼ 36) and Xenopus (Silurana) tropicalis (2n ¼ 20) are good animal models for studying the process of genomic and chromosomal reorganization after WGD because X. laevis is an allotetraploid species that resulted from WGD after the interspecific hybridization of diploid species closely related to X. tropicalis. We constructed a comparative cytogenetic map of X. laevis using 60 complimentary DNA clones that covered the entire chromosomal regions of 10 pairs of X. tropicalis chromosomes. We consequently identified all nine homoeologous chromosome groups of X. laevis. Hybridization signals on two pairs of X. laevis homoeologous chromosomes were detected for 50 of 60 (83%) genes, and the genetic linkage is highly conserved between X. tropicalis and X. laevis chromosomes except for one fusion and one inversion and also between X. laevis homoeologous chromosomes except for two inversions. These results indicate that the loss of duplicated genes and inter-and/or intrachromosomal rearrangements occurred much less frequently in this lineage, suggesting that these events were not essential for diploidization of the allotetraploid genome in X. laevis after WGD.

Chromosome Banding in Amphibia. XXXII. The Genus Xenopus (Anura, Pipidae)

“…In their pioneering cytogenetic work on the genus Xenopus , Janina Tymowska and co-workers (for references, see table 1 ) did not arrange the ordinarily stained chromosomes according to decreasing lengths, but established sophisticated standard karyotypes which were based on the relative sizes of short and long chromosome arms. Subsequently, these unconventional chromosome groupings were adopted by others in studies on chromosome banding [Sekiya and Nakagawa, 1983;Schmid et al, 1987;Schmid and Steinlein, 1991], chromosome painting [Krylov et al, 2010] and mapping of genes and repetitive DNA sequences [Courtet et al, 2001;Krylov et al, 2003Krylov et al, , 2007Tlapakova et al, 2005;Nanda et al, 2008;Uno et al, 2008Uno et al, , 2013. In the present study, this system is simplified and the chromosomes are arranged according to the new nomenclature of Xenopus chromosomes established by the Xenopus Gene Nomenclature Committee [Matsuda et al, this issue].…”

“…a Quartets formed after Schmid and Steinlein [1991]. b Quartets formed after Uno et al [2013]. type showing groups of 4 chromosomes (quartets).…”

“…Following this very first trial, studies using Zoo-FISH with 8 probes obtained from X. tropicalis [Krylov et al, 2010], as well as FISH with 60 cDNA clones of X. laevis [Uno et al, 2013] were used to identify the exact tetraploid X. laevis karyotype. The 9 quartets identified by Uno et al [2013] are shown in figure 5 b.…”

Nucleolar dominance and maternal control of 45S rDNA expression

“…For example, additional smaller clusters of 45S rRNA genes on other chromosomes may go undetected, creating a more complex rDNA landscape shifting expression from one direction to another. Indeed, Xenopus are pseudo-polyploids with very complex genomes [43], and even though they have lost 50 -75% of all duplicated genes [44], remnants of 45S rRNA clusters may exist in addition to the main NOR.…”

The sea lamprey meiotic map improves resolution of ancient vertebrate genome duplications

“…However, we acknowledge that the simplest explanation may not always be correct. If microchromosome-associated duplications are, in reality, the product of a gnathostome-specific WGD (i.e., 2R), then the evolutionary assortment of post-2R chromosomes must have progressed in a manner that is substantially different from other vertebrate whole-genome duplication events (i.e., in the Xenopus lineage) [Evans et al 2004;Uno et al 2013], in the salmonid lineage [Berthelot et al 2014], or near the base of the teleost fish lineage ). Under a hypothetical 2R, the evolutionary assortment of post-2R chromosomes would have involved large-scale loss of chromosomes and chromosomal segments, rather than the gradual diversification and nearly random mutational loss of paralogs.…”