Not necessarily all cells of an organism contain the same genome. Some eukaryotes exhibit dramatic differences between cells of different organs, resulting from programmed elimination of chromosomes or their fragments. Here, we present a detailed analysis of programmed B chromosome elimination in plants. Using goatgrass Aegilops speltoides as a model, we demonstrate that the elimination of B chromosomes is a strictly controlled and highly efficient root-specific process. At the onset of embryo differentiation B chromosomes undergo elimination in proto-root cells. Independent of centromere activity, B chromosomes demonstrate nondisjunction of chromatids and lagging in anaphase, leading to micronucleation. Chromatin structure and DNA replication differ between micronuclei and primary nuclei and degradation of micronucleated DNA is the final step of B chromosome elimination. This process might allow root tissues to survive the detrimental expression, or overexpression of B chromosome-located root-specific genes with paralogs located on standard chromosomes. B chromosomes are supernumerary chromosomes exhibiting dramatic differences between different organs in same species. Here, the authors show programmed B chromosome elimination in goatgrass starts at the onset of embryo differentiation by nondisjunction of chromatids, anaphase lagging, and ends with the degradation of micronucleated DNA.

/pdf/supernumerary-b-chromosomes-of-aegilops-speltoides-undergo-c3tkw60zml.pdf

Supernumerary B chromosomes of Aegilops speltoides undergo precise elimination in roots early in embryo development

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

Evolution and biology of supernumerary B chromosomes.

Despite possessing multiple sets of related (homoeologous) chromosomes, hexaploid wheat (Triticum aestivum) restricts pairing to just true homologs at meiosis. Deletion of a single major locus, Pairing homoeologous1 (Ph1), allows pairing of homoeologs. How can the same chromosomes be processed as homologs instead of being treated as nonhomologs? Ph1 was recently defined to a cluster of defective cyclin-dependent kinase (Cdk)-like genes showing some similarity to mammalian Cdk2. We reasoned that the cluster might suppress Cdk2-type activity and therefore affect replication and histone H1 phosphorylation. Our study does indeed reveal such effects, suggesting that Cdk2-type phosphorylation has a major role in determining chromosome specificity during meiosis.

/pdf/the-ph1-locus-suppresses-cdk2-type-activity-during-1wece9i96x.pdf

The Ph1 Locus Suppresses Cdk2-Type Activity during Premeiosis and Meiosis in Wheat

B chromosomes (Bs) are dispensable components of the genomes of numerous species. In contrast with the prevalent view that Bs do not harbor genes, our recent sequence analysis revealed that Bs of rye (Secale cereale) are rich in gene-derived sequences. We compared these gene-like fragments of the rye B with their ancestral A-located counterparts and confirmed an A chromosomal origin and the pseudogenization of B-located gene-like fragments. About 15% of the pseudogene-like fragments on Bs are transcribed in a tissue-type and genotype-specific manner. In addition, B-located sequences can cause in trans down- or upregulation of A chromosome–encoded genic fragments. Phenotypes and effects associated with the presence of Bs might be explained by the activity of B-located pseudogenes. We propose a model for the evolution of B-located pseudogenes.

/pdf/formation-and-expression-of-pseudogenes-on-the-b-chromosome-3ovveonw6n.pdf

Formation and Expression of Pseudogenes on the B Chromosome of Rye

B chromosomes (Bs) are supernumerary chromosomes that vary in number among individuals of the same species. Because of their dispensable nature, their non-Mendelian inheritance and their origin from A chromosomes (As), one might assume that Bs followed a different evolutionary pathway from As, this being reflected in differences in their high-copy DNA constitution. We provide detailed insight into the composition and distribution of rye (Secale cereale) B-located high-copy sequences. A- and B-specific high-copy sequences were identified in silico. Mobile elements and satellite sequences were verified by fluorescence in situ hybridization (FISH). Replication was analyzed via EdU incorporation. Although most repeats are similarly distributed along As and Bs, several transposons are either amplified or depleted on the B. An accumulation of B-enriched satellites was found mostly in the nondisjunction control region of the B, which is transcriptionally active and late-replicating. All B-enriched sequences are not unique to the B but are also present in other Secale species, suggesting the origin of the B from As of the same genus. Our findings highlight the differences between As and Bs. Although Bs originated from As, they have since taken a separate evolutionary pathway.

https://nph.onlinelibrary.wiley.com/doi/pdf/10.1111/nph.12289

High-copy sequences reveal distinct evolution of the rye B chromosome.

The rye B chromosome is a supernumerary chromosome that increases in number in its host by directed postmeiotic drive. Two types of rye B chromosomes that had been introduced into common wheat were dissected into separate segments by the gametocidal system to produce a number of rearranged B chromosomes, such as telosomes, terminal deletions and translocations with wheat chromosomes. A total of 13 dissected B chromosomes were isolated in common wheat, and were investigated for their nondisjunction. properties. Rearranged B chromosomes, separated from their B-specific repetitive sequences on the distal part of the long arm, did not undergo nondisjunction, and neither did a translocated wheat chromosome carrying a long-arm distal segment containing the B-specific repetitive sequences. However, such rearranged B chromosomes, missing their B-specific sequences could undergo nondisjunction when they coexisted with the standard B chromosome or a wheat chromosome carrying the B-specific sequences. Deficiencies of the short arm did not completely abolish the nondisjunction properties of the B chromosome, but did reduce the frequency of nondisjunction. These results confirmed previous suggestions that the directed nondisjunction of the rye B chromosome is controlled by two elements, pericentromeric sticking sites and a trans-acting element carried at the distal region of the long arm of the B chromosome. Additionally, it is now shown that the distal region of the long arm of the B chromosome which provides this function is that which carries the B-specific repetitive sequences.

Hishashi Tsujimoto

Papers

Dissection of rye B chromosomes, and nondisjunction properties of the dissected segments in a common wheat background