Mechanisms of the evolutionary chromosome plasticity: Integrating the ‘Centromere-from-Telomere' hypothesis with telomere length regulation

Abstract

The “centromere from-telomere-hypothesis” proposed by Villasante et al., [2007, Proc Natl Acad Sci USA, 104, 10542-47] aims to explain the evolutionary origin of the eukaryotic chromosome. The hypothesis is based on the notion that the process of eukaryogenesis was initiated by the adaptive responses of the symbiont eubacterium and its archaeal host to their new conditions. The adaptive response included fragmentation of the circular genome of the host into multiple linear fragments with free DNA ends. The action of mobile genetic elements stabilized free DNA ends resulting in the formation of proto-telomeres. Sequences next to proto-telomeres, the sub-telomeric sequences, were immediately targeted as the new cargo by the tubulin-based cytoskeleton thus becoming proto-centromeres. A period of genomic instability followed. Eventually, functioning centromeres and telomeres emerged heralding the arrival of the eukaryotic chromosome in the evolution. This paper expands the “centromere-from-telomere” hypothesis by integrating it with two sets of data: chromosome-specific telomere length distribution and chromomere size gradient. The integration adds a new dimension to the hypothesis but also provides an insight into the mechanisms of chromosome plasticity underlying the karyotype evolution.