Evolution and biology of supernumerary B chromosomes

Abstract

B chromosomes (Bs) are dispensable components of the genome exhibiting non-Mendelian inheritance and have been widely reported on over several thousand eukaryotes, but still remain an evolutionary mystery ever since their first discovery over a century ago [1]. Recent advances in genome analysis have significantly improved our knowledge on the origin and composition of Bs in the last few years. In contrast to the prevalent view that Bs do not harbor genes, recent analysis revealed that Bs of sequenced species are rich in gene-derived sequences. We summarize the latest findings on supernumerary chromosomes with a special focus on the origin, DNA composition, and the non-Mendelian accumulation mechanism of Bs.

Fig. 1

Examples of plant and animal species possessing B chromosomes. a The Bs in rye (Secale cereale). Arrowed Bs showing cross-hybridization with the B-specific repeat ScCl11 (red), Sc36c82 (green), and D1100 (yellow). (Picture provided by A. Marques, Gatersleben, Germany.) b The micro and standard Bs (arrowed) in Brachycome dichromosomatica. Metaphase chromosomes showing cross-hybridization with 45S rDNA (green). c The Bs (arrowed) in Crepis capillaris. Metaphase chromosomes showing cross-hybridization with 45S rDNA (red) and Arabidopsis-type telomere probes (green) probe obtained from microdissected Bs. d The Bs in Korean field mouse (Apodemus peninsulae): two-color FISH of microdissected DNA probes derived from centromeric C-positive region of autosome (red) and from C-negative region of the arm of one of the Bs (green) with metaphase chromosomes of specimens containing 18 Bs. Arrows indicate the dot-like Bs; sex chromosomes are marked with X and Y. (Picture provided by N.B. Rubtsov, Novosibirsk, Russia.) e The Bs in migratory locust (Locusta migratoria). Mitotic metaphase from a female embryo showing cross-hybridization with a DNA probe obtained from microdissected Bs. Note the intense painting of the B chromosomes (arrowed) and the pericentromeric regions of several of the 24 A chromosomes. (Picture provided by J.P.M. Camacho, Granada, Spain.) f The Bs in rye (Secale cereale). Arrowed Bs showing cross-hybridization with mitochondrial DNA (blue), plastid DNA (green) and the B-specific D1100 repeat (yellow). Insets show Bs after hybridization with (f′) plastid DNA (green) or (f″) mitochondrial DNA (blue). Note that only 12 of 14 A chromosomes are shown

Fig. 2

Model of the evolution of a B chromosome. 1 Translocation chromosome derived from duplicated A chromosome fragments results in 2 a decay of meiotic A–B pairing and the formation of a proto-B. 3 The accumulation of organellar and A chromosome-derived DNA fragments, amplification of B-specific repeats, erosion and inactivation of A-derived genes (Muller’s ratchet) and the gain of chromosome drive forms a B chromosome

Fig. 3

Model of the evolution of B-located pseudogenes. The B chromosome descends from A chromosome(s) after spontaneous whole or partial genome duplication. Proto-B still shows sequence similarity to the parental A chromosome(s). A proposed gene dosage compensation mechanism suppresses activity of B-located genes. Finally, B-located gene sequences became pseudogenized by mutations and accumulation of mobile and satellite DNA