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.

Keywords: cenH3; centromere; holocentric chromosomes; kinetochore; meiosis; mitosis; neocentromeres; plants.

FIGURE 1

Structure and behavior of a monocentric and a holocentric chromosome. (A) A metacentric chromosome shows a primary constriction during metaphase. During anaphase chromatids move as V-shaped structures due to microtubule attachment to the size-restricted centromere. (B) A holocentric chromosome shows an almost chromosome-wide centromere extension and no primary constriction during metaphase. Sister chromatids are not discernible. During anaphase spindle microtubule attachment to the holocentromere results in chromatids moving as linear bars parallel to the spindle. Inset, various centromeric subdomains fuse to one functional composite linear holocentromere at metaphase. (C) Breakage of a monocentric chromosome results in loss of the acentric chromosome fragment during anaphase, whereas (D) after chromosome breakage of a holocentric chromosome both fragments retain kinetic activity due to the almost chromosome-wide centromere extension and thus can be transmitted. Note absence of telomeric repeats at broken chromosome ends. In case of holocentric chromosomes of Luzula elegans, rapid telomere-mediated “chromosome healing” occurs (Jankowska et al., 2015).

FIGURE 2

Schematic representation of chromosomes with multiple centromeres. (A) A chromosome with two active centromeres (di-centromere or dicentric chromosome) is typically unstable. A twist between sister chromatids within the region between both centromeres leads to merotelic spindle attachment to two kinetochores on the same chromatid resulting in an anaphase bridge and subsequent chromosome breakage. (B,C) Stabilization of a dicentric chromosome can occur by (B) inactivation of one centromere, so that the chromosome behaves as monocentric or (C) when the close proximity between two active centromeres enables them to behave as one functional unit. (D) Meta-polycentric chromosome with three functional centromeres within one constriction.

FIGURE 3

Formation and behavior of de novo centromeres. (A) Following chromosome breakage, an acentric fragment can form a neocentromere allowing its proper transmission. (B) Chromosome breakage close to the endogenous centromere may lead to neocentromere formation due to presence or spreading of centromeric marks (e.g., cenH3) to pericentromeric regions. (C) Neocentromere formation in an intact chromosome leads to a dicentric chromosome structure. If this results in chromosome breakage, a centromere- and a neocentromere-containing fragment will result.

FIGURE 4

Schematic representation of meiosis-specific neocentromeres in plants. (A) During anaphase II, terminal neocentromeres are visible as heterochromatic stretches directed toward the cell poles ahead of the centromere. Telomeric regions are not stretched to the poles. Large heterochromatic regions (represented as larger yellow circles) are more prone to form neocentromeres than small ones. (B) Neocentromere in rye 5RL arises at an interstitial heterochromatic constriction and can substitute for the centromere during anaphase I.