Inference of the Protokaryotypes of Amniotes and Tetrapods and the Evolutionary Processes of Microchromosomes from Comparative Gene Mapping

Abstract

Comparative genome analysis of non-avian reptiles and amphibians provides important clues about the process of genome evolution in tetrapods. However, there is still only limited information available on the genome structures of these organisms. Consequently, the protokaryotypes of amniotes and tetrapods and the evolutionary processes of microchromosomes in tetrapods remain poorly understood. We constructed chromosome maps of functional genes for the Chinese soft-shelled turtle (Pelodiscus sinensis), the Siamese crocodile (Crocodylus siamensis), and the Western clawed frog (Xenopus tropicalis) and compared them with genome and/or chromosome maps of other tetrapod species (salamander, lizard, snake, chicken, and human). This is the first report on the protokaryotypes of amniotes and tetrapods and the evolutionary processes of microchromosomes inferred from comparative genomic analysis of vertebrates, which cover all major non-avian reptilian taxa (Squamata, Crocodilia, Testudines). The eight largest macrochromosomes of the turtle and chicken were equivalent, and 11 linkage groups had also remained intact in the crocodile. Linkage groups of the chicken macrochromosomes were also highly conserved in X. tropicalis, two squamates, and the salamander, but not in human. Chicken microchromosomal linkages were conserved in the squamates, which have fewer microchromosomes than chicken, and also in Xenopus and the salamander, which both lack microchromosomes; in the latter, the chicken microchromosomal segments have been integrated into macrochromosomes. Our present findings open up the possibility that the ancestral amniotes and tetrapods had at least 10 large genetic linkage groups and many microchromosomes, which corresponded to the chicken macro- and microchromosomes, respectively. The turtle and chicken might retain the microchromosomes of the amniote protokaryotype almost intact. The decrease in number and/or disappearance of microchromosomes by repeated chromosomal fusions probably occurred independently in the amphibian, squamate, crocodilian, and mammalian lineages.

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

“…Based on our previous mapping data of 140 genes in X. tropicalis (Uno et al, 2012), we selected 60 genes, which covered the entire chromosomal regions of 10 pairs of X. tropicalis chromosomes, for their comparative mapping to X. laevis chromosomes (XLA) (Figure 2 and Table 1). The identification of each chromosome and subchromosomal localization of the hybridization signals was performed using the Hoechst G-banded ideogram.…”

“…For chromosome mapping, 60 X. laevis cDNA clones were selected from 140 clones that were used for the chromosome mapping of X. tropicalis in our previous study (Uno et al, 2012). These clones were isolated based on a web data catalog of the NIBB/NIG/NBRP Xenopus laevis EST project (XDB3, http:// xenopus.nibb.ac.jp/).…”

“…a Human gene symbol. b Clone numbers of X. laevis EST clones used for mapping, which were selected from a web data catalog of the NIBB/NIG/NBRP Xenopus laevis EST project (XDB3, http://xenopus.nibb.ac.jp/) based on the X. tropicalis chromosome map described by Uno et al (2012). Fragment sizes of all X. laevis EST clones were 41.5 kb.…”

“…Therefore, X. laevis and X. tropicalis are good animal models for understanding the process of genomic and chromosomal reorganization after WGD. We recently constructed a high-resolution chromosome map consisting of 140 genes for X. tropicalis (Uno et al, 2012). The draft genome assemblies of X. tropicalis were reported previously (Hellsten et al, 2010), and several comparative studies of complimentary DNA (cDNA) sequences have been performed between X. tropicalis and X. laevis (Morin et al, 2006;Hellsten et al, 2007;Sémon and Wolfe, 2008).…”

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

“…Previous studies have shown that microchromosomes are present in most major gnathostome lineages and that they represent distinct evolutionarily conserved entities at least to the base of the tetrapod lineage (∼350 Mya) (Voss et al 2011;Uno et al 2012). Several of these microchromosomes: GG28 (ancA), GG20, 23 (ancB), GG13, 22 (ancC), GG26 (ancD), and GG27, 29 (ancE), bear the signature of duplication and fission events that are temporally distinct from 1R.…”