Holocentric chromosomes: convergent evolution, meiotic adaptations, and genomic analysis

Abstract

In most eukaryotes, the kinetochore protein complex assembles at a single locus termed the centromere to attach chromosomes to spindle microtubules. Holocentric chromosomes have the unusual property of attaching to spindle microtubules along their entire length. Our mechanistic understanding of holocentric chromosome function is derived largely from studies in the nematode Caenorhabditis elegans, but holocentric chromosomes are found over a broad range of animal and plant species. In this review, we describe how holocentricity may be identified through cytological and molecular methods. By surveying the diversity of organisms with holocentric chromosomes, we estimate that the trait has arisen at least 13 independent times (four times in plants and at least nine times in animals). Holocentric chromosomes have inherent problems in meiosis because bivalents can attach to spindles in a random fashion. Interestingly, there are several solutions that have evolved to allow accurate meiotic segregation of holocentric chromosomes. Lastly, we describe how extensive genome sequencing and experiments in nonmodel organisms may allow holocentric chromosomes to shed light on general principles of chromosome segregation.

Absence of positive selection on CenH3 inLuzulasuggests that holokinetic chromosomes may suppress centromere drive

“…2) and, as previously speculated, that holokinetism itself might have evolved as a defence against centromere drive (Talbert et al, 2008;Malik and Henikoff, 2009;Bures et al, 2013). Accordingly, although holokinetism has evolved independently in various lineages of plants and animals (Melters et al, 2012), it appears to have evolved only in lineages with asymmetric meiosis where the need for a defence against centromere drive can be assumed, not in lineages with symmetric meiosis, such as bryophytes, lycophytes, ferns, horsetails or fungi (Bures et al, 2013), where such a defence has no sense. Nevertheless, even if centromere drive is suppressed in holokinetic lineages, holokinetism is likely to provide an opportunity for a different kind of meiotic drive propelling divergence in chromosomal size and number -holokinetic drive (Bures and Zedek, 2014;Escudero et al, 2015).…”

The 19S proteasome subunit Rpt3 regulates distribution of CENP-A by associating with centromeric chromatin

“…Deviation in the size of a centromere would result in formation of an abnormally sized kinetochore, which could not interact with the spindle properly 6 . In most eukaryotes, with the exception of holocentric species 7 , each chromosome contains a single distinct centromere. A chromosome experimentally forced to have an additional centromere undergoes successive rounds of anaphase bridge formation and breakage in budding yeast and fly [8][9][10] .…”

Interplay Between Spindle Architecture and Function

“…Holocentric chromosomes have the unusual property of assembling kinetochore complexes and attaching to MTs along their entire length. Although best characterized in the nematode Caenorhabditis elegans, holocentric chromosomes are found in a broad range of plant and animal species (Melters et al, 2012). Despite variation in their number and organization, a common feature of k-fiber MTs is that they are resistant to treatments that depolymerize other spindle MTs, such as cold temperature or low doses of MT-depolymerizing drugs.…”