Comprehending the dynamism of B chromosomes in their journey towards becoming unselfish

Abstract

Investigated for more than a century now, B chromosomes (Bs) research has come a long way from Bs being considered parasitic or neutral to becoming unselfish and bringing benefits to their hosts. B chromosomes exist as accessory chromosomes along with the standard A chromosomes (As) across eukaryotic taxa. Represented singly or in multiple copies, B chromosomes are largely heterochromatic but also contain euchromatic and organellar segments. Although B chromosomes are derived entities, they follow their species-specific evolutionary pattern. B chromosomes fail to pair with the standard chromosomes during meiosis and vary in their number, size, composition and structure across taxa and ensure their successful transmission through non-mendelian mechanisms like mitotic, pre-meiotic, meiotic or post-meiotic drives, unique non-disjunction, self-pairing or even imparting benefits to the host when they lack drive. B chromosomes have been associated with cellular processes like sex determination, pathogenicity, resistance to pathogens, phenotypic effects, and differential gene expression. With the advancements in B-omics research, novel insights have been gleaned on their functions, some of which have been associated with the regulation of gene expression of A chromosomes through increased expression of miRNAs or differential expression of transposable elements located on them. The next-generation sequencing and emerging technologies will further likely unravel the cellular, molecular and functional behaviour of these enigmatic entities. Amidst the extensive fluidity shown by B chromosomes in their structural and functional attributes, we perceive that the existence and survival of B chromosomes in the populations most likely seem to be a trade-off between the drive efficiency and adaptive significance versus their adverse effects on reproduction.

Keywords: B chromosomes; adaptive significance; genetic drive; non-disjunction; non-mendelian transmission; preferential fertilization.

FIGURE 1

Depiction of various proposed models on the origin of B chromosomes:(A) genomic DNA amalgamated from multiple A chromosomes undergo structural rearrangements like translocation, duplication, transposition, insertion of repeat sequences and pericentromeric regions followed by the addition of a few B essential genes required for their successful transmission and chromatin reorganizing genes resulting in the formation of a nascent Proto-B chromosome. The Proto-B chromosome is further modified by the addition of transposable elements and DNA sequences from the organellar genome and ampliconic multiple A chromosome sequences to form a mature stable B chromosome with diverse functions. (B) the pseudoautosomal region (PAR) on X and Y chromosomes undergoes double-stranded breaks which in association with the centromere leads to the formation of neo-B chromosome. (C) One homologue of the A chromosome pair which has a secondary constriction on its short arm undergoes inversion and centromeric fission. The fission portion of the short arm inverts again without joining back at the same position resulting in the formation of an A chromosome without secondary constriction and a newly formed B chromosome which is further stabilized by the incorporation of many other types of DNA fragments. (D) ancestral A chromosome has a few hotspot regions which undergo breakage forming a chromosome without a telomeric end. This broken chromosome can either form a new telomeric end or the broken arms of the chromosome fuse following the inactivation of the centromere. Both mechanisms finally result in the formation of B chromosome (E) triplo 2 is a translocation trisome of chromosome 2 in Plantago lagopus in which rDNA regions 18S, 5.8S, 25S and 5S undergo breakage, and fragmentation followed by fusion with centromeric fragments to form a nascent mini B chromosome. Subsequently, there is selective amplification of 5S region along with the addition of telomeric repeats followed by misdivision of centromere leading to the formation of an iso-chromosome type of B.

FIGURE 2

Functional aspects of genes identified on B chromosomes in various organisms.

FIGURE 3

Mechanism of evolution of B chromosomes: The A chromosome-derived Bs acquire diverse types of DNA sequences. Certain variant/mutated genes of the A genome suppress the parasitic gene on B and neutralize their harmful effects. The B-parasitic gene, however, is essential for its drive. There may be three outcomes of this suppression mechanism. (1) Genes on B chromosomes do not undergo any mutation, and remain switched off eventually resulting in loss of B drive furthering their extinction (2) Parasitic gene on B chromosome undergoes mutation and gets switched on to overcome the neutralizing effects of the A variant genes. This revives the B drive mechanism leading to the regeneration of B chromosomes (3) Both the parasitic and useful genes on B chromosome undergo mutations and get switched on. As a result, the drive mechanism becomes active and Bs are regenerated and the useful gene expresses itself leading to a new phenotype that provides adaptive evolutionary advantage to the host harboring this useful mutated gene.