Telomere-Centric Genome Repatterning Determines Recurring Chromosome Number Reductions during the Evolution of Eukaryotes

Whole-genome duplication (WGD) is central to the evolution of many eukaryotic genomes, in particular rendering angiosperm (flowering plant) genomes much less stable than those of animals. Following repeated occurrence of polyploidies, angiosperm chromosome numbers have usually been restored to a narrow range, possibly contributing to the recovery of diploid heredity.  Here we proposed a telomere-centric model to describe genome repatterning after polyploidization. In several angiosperms affected by WGD, we showed that chromosome number reduction (CNR) was best explained by intra- and/or inter-chromosomal crossovers to form new chromosomes that utilize the existing telomeres of ‘invaded’ and centromeres of ‘invading’ chromosomes, the alternative centromeres and telomeres being lost. Comparison to the banana genome supports a ‘fusion model’ for the evolution of rice chromosomes 2 and 3, implying that the grass common ancestor had 7 chromosomes rather than the 5 implied by a ‘fission model.’ The ‘invading’ and ‘invaded’ chromosomes are frequently homoeologs, originating from duplication of a common ancestral chromosome and with greater-than-average DNA-level correspondence to one another. We produced movies to show how grass and Arabidopsis genomes were reconstructed. Telomere-centric genome repatterning  revealed in plants may be a general mechanism of restoring small linear chromosome numbers in higher eukaryotes.