Origin and Evolution of B Chromosomes in the Cichlid Fish Astatotilapia latifasciata Based on Integrated Genomic Analyses

Abstract

Approximately 15% of eukaryotes contain supernumerary B chromosomes. When present, B chromosomes frequently represent as much as 5% of the genome. Despite thousands of reports describing the distribution of supernumeraries in various taxa, a comprehensive theory for the origin, maintenance, and evolution of B chromosomes has not emerged. Here, we sequence the complete genomes of individual cichlid fish (Astatotilapia latifasciata) with and without B chromosomes, as well as microdissected B chromosomes, to identify DNA sequences on the B. B sequences were further analyzed through quantitative polymerase chain reaction and in situ hybridization. We find that the B chromosome contains thousands of sequences duplicated from essentially every chromosome in the ancestral karyotype. Although most genes on the B chromosome are fragmented, a few are largely intact, and we detect evidence that at least three of them are transcriptionally active. We propose a model in which the B chromosome originated early in the evolutionary history of Lake Victoria cichlids from a small fragment of one autosome. DNA sequences originating from several autosomes, including protein-coding genes and transposable elements, subsequently inserted into this proto-B. We propose that intact B chromosome genes involved with microtubule organization, kinetochore structure, recombination and progression through the cell cycle may play a role in driving the transmission of the B chromosome. Furthermore, our work suggests that karyotyping is an essential step prior to genome sequencing to avoid problems in genome assembly and analytical biases created by the presence of high copy number sequences on the B chromosome.

Molecular Analysis of the B Microchromosome in <b><i>Steindachnerina insculpta</i></b> (Characiformes: Curimatidae) by Microdissection

“…3 E-G) . Houben et al [1996] postulated that the presence of homologous sequences between A and B chromosomes allows inferring an origin by fragmentation for the B chromosome, and this was confirmed by Valente et al [2014] in fishes. Probably, the same occurred in the studied species, considering the homology between the B and A chromosomes and the presence of the B signal on more than one A chromosome ( fig.…”

“…The wide distribution of DIRS elements suggests that the group of these retroelements arose in early eukaryote evolution [Goodwin and Poulter, 2004]. In Astatotilapia latifasciata , studies of the behavior of the retroelements Rex1 and Rex3 by in situ hybridization allowed the authors to suggest that the B chromosome evolved from small chromosomal fragments followed by the invasion of the proto-B chromosome by several repeated DNA families [Fantinati et al, 2011;Valente et al, 2014]. Although Rex and DIRS retrotransposons have different structures, the same mechanism probably happened to the B chromosome of S. insculpta .…”

“…In Astatotilapia latifasciata (Regan, 1929), the chromosomal mapping of the C 0 t-1 DNA fraction, retrotransposons, and ribosomal DNA sequences enabled the authors to suggest that B chromosomes may have evolved from small fragments followed by an invasion of the proto-B chromosome by several families of repetitive DNA [Fantinati et al, 2011;Valente et al, 2014]. Cytogenetic and genomic analysis led the authors to propose that these B chromosomes originated early in the evolutionary history of cichlids.…”

Chromosomal Mapping of Repeat DNA in <b><i>Bergiaria westermanni</i></b> (Pimelodidae, Siluriformes): Localization of 45S rDNA in B Chromosomes

“…The chromosome pair 27 carries these 2 types of sequence, suggesting that B chromosomes originated from this pair. However, it is also possible that these repetitive sequences were incorporated after the origin of one B chromosome, as proposed by Valente et al [2014]. In this model, DNA sequences from A elements are transferred to B chromosomes by nonhomologous recombination, reverse transcription, transposable element invasion, and duplication of single-copy sequences by a drive in the transposable element invasion [Clark et al, 2017].…”

<b><i>Plantago lagopus </i></b>B Chromosome Is Enriched in 5S rDNA-Derived Satellite DNA

“…Recent studies in rye [Martis et al, 2012] and in the fish species Astatotilapia latifasciata [Valente et al, 2014] using next-generation sequencing and sophisticated bioinformatics tools showed that in these species Bs had originated from multiple As, most likely by a pathway involving partial genome duplication, chromosome rearrangements, accumulation of organellar-derived DNA, and sequence amplification. Similarly, analysis of evolutionarily conserved A chromosome segments in wild canid species identified several regions of domestic dog A chromosome sequences that share sequence similarity with canid B chromosomes [Becker et al, 2011].…”