Atypical centromeres in plants—what they can tell us

Abstract

The centromere, visible as the primary constriction of condensed metaphase chromosomes, is a defined chromosomal locus essential for genome stability. It mediates transient assembly of a multi-protein complex, the kinetochore, which enables interaction with spindle fibers and thus faithful segregation of the genetic information during nuclear divisions. Centromeric DNA varies in extent and sequence composition among organisms, but a common feature of almost all active eukaryotic centromeres is the presence of the centromeric histone H3 variant cenH3 (a.k.a. CENP-A). These typical centromere features apply to most studied species. However, a number of species display “atypical” centromeres, such as holocentromeres (centromere extension along almost the entire chromatid length) or neocentromeres (ectopic centromere activity). In this review, we provide an overview of different atypical centromere types found in plants including holocentromeres, de novo formed centromeres and terminal neocentromeres as well as di-, tri- and metapolycentromeres (more than one centromere per chromosomes). We discuss their specific and common features and compare them to centromere types found in other eukaryotic species. We also highlight new insights into centromere biology gained in plants with atypical centromeres such as distinct mechanisms to define a holocentromere, specific adaptations in species with holocentromeres during meiosis or various scenarios leading to neocentromere formation.

Restructuring of Holocentric Centromeres During Meiosis in the Plant Rhynchospora pubera

“…Accordingly, the occurrence of very few crossovers is reported for holocentric organisms, generally one or two per rod and ring bivalent, respectively, mostly located at the noncentromeric terminal regions (Cuacos et al 2015). This is also true for R. pubera, in which chiasmata occur terminally.…”

“…In addition, the extended holocentric kinetochore increases the risk of a stable attachment to microtubules from both poles of the spindle (merotelic attachment), and hence an aberrant segregation of chromosomes may occur. As adaptation, species with holocentric chromosomes have evolved different solutions during meiosis, such as a restricted kinetochore activity, ensuring canonical meiosis order, and "inverted meiosis," where a reverse order of sister chromatid and homolog separation occurs (see below) (reviewed in Viera et al 2009 andCuacos et al 2015).…”

Analysis of the small chromosomalPrionium serratum(Cyperid) demonstrates the importance of a reliable method to differentiate between mono- and holocentricity

“…In large chromosome species like L. elegans and R. pubera, holocentromeres form at somatic pro-and metaphase a distinct longitudinal groove along each sister chromatid which is visible by standard (Heckmann et al, 2011;Nagaki et al, 2005), structured illumination microscopy and scanning electron microscopy (Marques et al, 2015;Wanner et al, 2015). The analysis of meiotic chromosome dynamics has been used to determine holocentricity in species with moderate to large chromosomes (reviewed in ((Cuacos et al, 2015); ). Three principle options exist to deal with holocentricity during meiosis: (i) 'chromosome remodelling', (ii) 'functional monocentricity' and (iii) 'inverted meiosis'.…”

Impact of parasitic lifestyle and different types of centromere organization on chromosome and genome evolution in the plant genusCuscuta

“…Genome sizes of most plant genera vary less than 10-fold, while a 100-fold variation has only been described for much broader taxonomic levels, like tribes or families (Pellicer et al, 2014;. Similarly, a holocentric chromosome organization is usually shared within whole families, like Cyperaceae (Cuacos et al, 2015), and thus the closest related taxa possessing monocentric chromosomes are phylogenetically distant.…”