Evolution of holocentric chromosomes: Drivers, diversity, and deterrents

Centromeres are specialized chromosomal regions that recruit kinetochore proteins and mediate spindle microtubule attachment to ensure faithful chromosome segregation during mitosis and meiosis. Centromeres can be restricted to one region of the chromosome. Named "monocentromere", this type represents the most commonly found centromere organization across eukaryotes. Alternatively, centromeres can also be assembled at sites chromosome-wide. This second type is called "holocentromere". Despite their early description over 100 years ago, research on holocentromeres has lagged behind that of monocentromeres. Nevertheless, the application of next generation sequencing approaches and advanced microscopic technologies enabled recent advances understanding the molecular organization and regulation of holocentromeres in different organisms. Here we review the current state of research on holocentromeres focusing on evolutionary considerations. First, we provide a brief historical perspective on the discovery of holocentric chromosomes. We then discuss models/drivers that have been proposed over the years to explain the evolutionary transition from mono- to holocentric chromosomes. We continue to review the description of holocentric chromosomes in diverse eukaryotic groups and then focus our discussion on a specific and recently characterized type of holocentromere organization in insects that functions independently of the otherwise essential centromeric marker protein CenH3, thus providing novel insights into holocentromere evolution in insects. Finally, we propose reasons to explain why the holocentric trait is not more frequent across eukaryotes despite putative selective advantages.