Drive and Gene Activity of a Selfish Chromosome

B chromosomes (Bs) are supernumerary components of the genome and do not confer any advantages on the organisms that harbor them. The maintenance of Bs in natural populations is possible by their transmission at higher than Mendelian frequencies. Nevertheless, the mechanism of B chromosome drive is largely unknown. Here, we show that the satellite-repeat enriched subterminal domain of rye (Secale cereale) Bs is controlling in trans the process of chromosome drive. Contrary to the heterochromatic regions of A chromosomes, this domain is simultaneously marked by trimethylated H3K4 and by trimethylated H3K27, an unusual combination of apparently conflicting histone modifications.  B-specific high copy repeat families of the nondisjunction control regions are producing long-non-coding RNA, although with different tissue type-dependent activity. The properties of nondisjunction control regions are conserved across different accessions and subspecies of rye. The accumulation process of the B is accompanied by centromere activity and is likely caused by extended cohesion of the B sister chromatids. Because of unequal spindle formation at the first pollen mitosis, nondisjoined B chromatids preferentially become located toward the generative pole. Also, our results indicated that rye B chromosome is originated from multiple A chromosomes. The repeat elements on A and B have different evolution and Bs were enriched in mitochondrial and plastid sequences and satellite repeats. Surprisingly the B chromosome has thousands of sequence reads with similarity to genes with known function. These genic sequences are partly active and were able to regulate the expression of A-located genes in trans.