B chromosomes of multiple species have intense evolutionary dynamics and accumulated genes related to important biological processes

Abstract

Background One of the biggest challenges in chromosome biology is to understand the occurrence and complex genetics of the extra, non-essential karyotype elements, commonly known as supernumerary or B chromosomes (Bs). The non-Mendelian inheritance and non-pairing abilities of B chromosomes make them an interesting model for genomics studies, thus bringing to bear different questions about their genetic composition, evolutionary survival, maintenance and functional role inside the cell. This study uncovers these phenomena in multiple species that we considered as representative organisms of both vertebrate and invertebrate models for B chromosome analysis. Results We sequenced the genomes of three animal species including two fishes Astyanax mexicanus and Astyanax correntinus, and a grasshopper Abracris flavolineata, each with and without Bs, and identified their B-localized genes and repeat contents. We detected unique sequences occurring exclusively on Bs and discovered various evolutionary patterns of genomic rearrangements associated to Bs. In situ hybridization and quantitative polymerase chain reactions further validated our genomic approach confirming detection of sequences on Bs. The functional annotation of B sequences showed that the B chromosome comprises regions of gene fragments, novel genes, and intact genes, which encode a diverse set of functions related to important biological processes such as metabolism, morphogenesis, reproduction, transposition, recombination, cell cycle and chromosomes functions which might be important for their evolutionary success. Conclusions This study reveals the genomic structure, composition and function of Bs, which provide new insights for theories of B chromosome evolution. The selfish behavior of Bs seems to be favored by gained genes/sequences.

A supernumerary “B-sex” chromosome drives male sex determination in the Pachón cavefish, Astyanax mexicanus

“…Pachó n cavefish B chromosomes are male-predominant B chromosomes Supernumerary B chromosomes (Bs) are generally thought to arise from the duplication and assembly of A chromosome sequences, [16][17][18][19] and their relationship to sex chromosomes has often been suspected and discussed. 15 Some hypotheses state that Bs are derived from sex chromosomes or, alternatively, evolved to become sex chromosomes.…”

“…15 Some hypotheses state that Bs are derived from sex chromosomes or, alternatively, evolved to become sex chromosomes. 15,[20][21][22][23] Because Bs have been described in A. mexicanus, 19,24,25 we performed cytogenetic analyses in 17 males and 11 females of a laboratory population of Pachó n cavefish (Pachó n) to investigate whether Pachó n Bs could be sex restricted. We found that Pachó n Bs are euchromatic mitotically unstable microchromosomes (Figures 1A, 1B, and S1) that are present in one to three copies in most male metaphases (mean number ± SD of Bs per male metaphase = 1.08 ± 0.41), contrasting with a barely detectable B occurrence in female metaphases (mean number ± SD of Bs per female metaphase = 0.05 ± 0.08; Figure 1C; Data S1A).…”

Impact of Repetitive DNA Elements on Snake Genome Biology and Evolution

“…During their evolution, variations in repeat sequences proliferate and mediate chromosomal rearrangements, resulting in either deleterious or positive effects. Consequently, repeats are interesting markers that can be used to study phylogenetic and taxonomic relationships [ 24 , 50 , 51 , 52 ]. The high level of specificity of repetitive sequences is an important tool for understanding evolutionary dynamics.…”

Long-term persistence of supernumerary B chromosomes in multiple species of Astyanax fish

“…The absence of this information precluded species-specific primer design and thus we cannot be sure whether negative qPCR results for some genes in these two species are due to gene absence in their B chromosomes or, as commented above, to sequence divergence in the gene regions were primers were designed to be anchored. A recent study has reported the gene content of B chromosomes in two more distantly related Astyanax species, namely A. correntinus and A. mexicanus [ 21 ], but the absence of coincidence with the four species studied here suggests an independent origin for B chromosomes in these two species.…”