Molecular cytogenetic differentiation of paralogs of Hox paralogs in duplicated and re-diploidized genome of the North American paddlefish (Polyodon spathula)

Abstract

Background: Acipenseriformes is a basal lineage of ray-finned fishes and comprise 27 extant species of sturgeons and paddlefishes. They are characterized by several specific genomic features as broad ploidy variation, high chromosome numbers, presence of numerous microchromosomes and propensity to interspecific hybridization. The presumed palaeotetraploidy of the American paddlefish was recently validated by molecular phylogeny and Hox genes analyses. A whole genome duplication in the paddlefish lineage was estimated at approximately 42 Mya and was found to be independent from several genome duplications evidenced in its sister lineage, i.e. sturgeons. We tested the ploidy status of available chromosomal markers after the expected rediploidization. Further we tested, whether paralogs of Hox gene clusters originated from this paddlefish specific genome duplication are cytogenetically distinguishable. Results: We found that both paralogs HoxA alpha and beta were distinguishable without any overlapping of the hybridization signal -each on one pair of large metacentric chromosomes. Of the HoxD, only the beta paralog was unequivocally identified, whereas the alpha paralog did not work and yielded only an inconclusive diffuse signal. Chromosomal markers on three diverse ploidy levels reflecting different stages of rediploidization were identified: quadruplets retaining their ancestral tetraploid condition, semi-quadruplets still reflecting the ancestral tetraploidy with clear signs of advanced rediploidization, doublets were diploidized with ancestral tetraploidy already blurred. Also some of the available microsatellite data exhibited diploid allelic band patterns at their loci whereas another locus showed more than two alleles. Conclusions: Our exhaustive staining of paddlefish chromosomes combined with cytogenetic mapping of ribosomal genes and Hox paralogs and with microsatellite data, brings a closer look at results of the process of rediploidization in the course of paddlefish genome evolution. We show a partial rediploidization represented by a complex mosaic structure comparable with segmental paleotetraploidy revealed in sturgeons (Acipenseridae). Sturgeons and paddlefishes with their high propensity for whole genome duplication thus offer suitable animal model systems to further explore evolutionary processes that were shaping the early evolution of all vertebrates.

The sterlet sturgeon genome sequence and the mechanisms of segmental rediploidization

“…Sturgeons are a group of rayfinned fish that diverged from the actinopterygian stem before the teleost-specific 3R duplication and after the ancient 2R event 4,5 . After their divergence from the other ray-finned fish, the various lineages of Acipenseriformes (sturgeon and paddlefish) experienced several polyploidization events 6 , resulting in karyotypes, comprising between ~120 chromosomes in some species, and ~360 chromosomes in species that are considered dodecaploid 7 . The genomic basis for this parallelism between basal and derived fish lineages to acquire WGDs is not clear.…”

Karyotype and chromosomal characteristics of rDNA of Cobitis strumicae Karaman, 1955 (Teleostei, Cobitidae) from Lake Volvi, Greece

“…The association of GC-rich DNA type of heterochromatin with rDNA sites is present in lower and higher teleostean groups, suggesting that it is evolutionarily conserved among teleosts ( Gornung 2013 ). However, this character exits also in bichirs ( Polypteriformes ), partly in paddlefishes ( Symonová et al 2017a ), gars ( Symonová et al 2017b ) and bowfin ( Majtánová et al 2017 ), but not in sturgeons ( Fontana et al 2007 ). Among Cobitis loaches, this characteristic pattern was found in C. vardarensis Karaman, 1928 ( Rábová et al 2001 ), C. elongatoides Băcescu et Mayer, 1969 ( Ráb et al 2000 ) and C. taenia Linnaeus, 1758 ( Boroň et al 2006 ), i.e.…”

Vertebrate Genome Evolution in the Light of Fish Cytogenomics and rDNAomics

“…However, to sequence and above all to assemble such genomes remains challenging (bichirs, lungfishes, sturgeons, salamanders). Hence, the “classical” cytogenetics still represents an important tool to analyze these genomes and the post-WGD evolution [ 20 , 89 , 108 ]. Not only in these cases, cytogenetics can largely benefit from genomics and bioinformatics and compensate for the obstacles during sequencing and genome assembling ([ 19 ], this special issue).…”