Selfish supernumerary chromosome reveals its origin as a mosaic of host genome and organellar sequences

Abstract

Supernumerary B chromosomes are optional additions to the basic set of A chromosomes, and occur in all eukaryotic groups. They differ from the basic complement in morphology, pairing behavior, and inheritance and are not required for normal growth and development. The current view is that B chromosomes are parasitic elements comparable to selfish DNA, like transposons. In contrast to transposons, they are autonomously inherited independent of the host genome and have their own mechanisms of mitotic or meiotic drive. Although B chromosomes were first described a century ago, little is known about their origin and molecular makeup. The widely accepted view is that they are derived from fragments of A chromosomes and/or generated in response to interspecific hybridization. Through next-generation sequencing of sorted A and B chromosomes, we show that B chromosomes of rye are rich in gene-derived sequences, allowing us to trace their origin to fragments of A chromosomes, with the largest parts corresponding to rye chromosomes 3R and 7R. Compared with A chromosomes, B chromosomes were also found to accumulate large amounts of specific repeats and insertions of organellar DNA. The origin of rye B chromosomes occurred an estimated ∼1.1-1.3 Mya, overlapping in time with the onset of the genus Secale (1.7 Mya). We propose a comprehensive model of B chromosome evolution, including its origin by recombination of several A chromosomes followed by capturing of additional A-derived and organellar sequences and amplification of B-specific repeats.

Fig. 1.

Multichromosomal origin of the rye B chromosome. (A) Rye B sequence reads mapped onto the barley genome. The heatmap depicts the detected homologous (syntenic) regions in the barley genome. Sequence reads were anchored on barley chromosomes 1H–7H using BLASTN and the best detectable match. Individual chromosomes are numbered. Multiple regions exhibit conserved genes with respect to barley chromosomes 2H, 3H, 4H, and 5H (implied syntenic regions) and multiple small regions on the remaining chromosomes. (B) Syntenic relationship between the A chromosomes of barley and rye. Chromosome 7R corresponds to regions from 2H, 4H, 5H ,and 7H (15). Thus, the B chromosome of rye shows extended similarity to regions of chromosomes 3R and 7R.

Fig. 2.

FISH of rye mitotic metaphase chromosomes with the centromeric retrotransposons Bilby (A), the B-specific pericentromeric Ty1/copia repeat CL11 (B), mitochondrial DNA (C), and plastid DNA (D). B chromosome-specific satellite repeats E3900 and D1100 were used for identifications of the Bs. The Bs are indicated by arrows. (Scale bar: 10 μm.)

Fig. 3.

Model of the stepwise evolution of the rye B chromosome after segmental genome duplication. (1) Reciprocal translocation of duplicated fragments of the 3R and 7R chromosomes and unbalanced segregation of a small translocation chromosome results in (2) 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 gain of chromosome drive resulted in the B chromosome.