Nuclear Envelope-Associated Chromosome Dynamics during Meiotic Prophase I

Abstract

Chromosome dynamics during meiotic prophase I are associated with a series of major events such as chromosomal reorganization and condensation, pairing/synapsis and recombination of the homologs, and chromosome movements at the nuclear envelope (NE). The NE is the barrier separating the nucleus from the cytoplasm and thus plays a central role in NE-associated chromosomal movements during meiosis. Previous studies have shown in various species that NE-linked chromosome dynamics are actually driven by the cytoskeleton. The linker of nucleoskeleton and cytoskeleton (LINC) complexes are important constituents of the NE that facilitate in the transfer of cytoskeletal forces across the NE to individual chromosomes. The LINCs consist of the inner and outer NE proteins Sad1/UNC-84 (SUN), and Klarsicht/Anc-1/Syne (KASH) domain proteins. Meiosis-specific adaptations of the LINC components and unique modifications of the NE are required during chromosomal movements. Nonetheless, the actual role of the NE in chromosomic dynamic movements in plants remains elusive. This review summarizes the findings of recent studies on meiosis-specific constituents and modifications of the NE and corresponding nucleoplasmic/cytoplasmic adaptors being involved in NE-associated movement of meiotic chromosomes, as well as describes the potential molecular network of transferring cytoplasm-derived forces into meiotic chromosomes in model organisms. It helps to gain a better understanding of the NE-associated meiotic chromosomal movements in plants.

Keywords: KASH proteins; SUN proteins; chromosome dynamics; cytoplasmic adaptors; meiosis prophase I; meiotic modification; nuclear envelope; nucleoplasmic adaptors.

Figure 1

The interphase structure of the NE. The NE consists of the inner nuclear membrane (INM), outer nuclear membrane (ONM) and the perinuclear space (PNS). The NE is embedded with nuclear pore complexes (NPCs), SUN proteins in the INM and KASH proteins in the ONM. LINC complexes are made of SUN proteins and KASH proteins, transferring cytoplasm-derived forces inti the chromosomes in the nucleoplasm. The ONM facing the cytoplasm is connected with the rough endoplasmic reticulum (rER). The nuclear lamina is a protein network that is situated close to the INM nucleoplasmic side. In plants, little is known about the nuclear lamina. However, electron microscopy has revealed there is an INM-associated dense meshwork, similar to the animal lamina.

Figure 2

Telomere movement at the NE during meiotic prophase. The four different movement classes are indicated as (A–D). Red dots indicate the positions of the telomeres relative to the NE. The relative direction of telomeric movements is indicated by black arrows. (A) Telomeres scattering in the nucleus move to the NE at the onset of leptotene stage. (B) Telomeres are tethered to the NE and stably connected to it at the late leptotene stage. The telomere clustering starts in the late leptotene stage, always overlaps with the zygotene stage and usually persists until pachytene. (C) The tightest clustering of telomeres is usually observed at the zygotene stage. (D) At pachytene, telomeres are motile and scattered over the NE again, while additional nuclear deformations and rotations occur (black arrows). For further information please see the Scherthan (2007).

Figure 3

A schematic representation of the link transferring cytoplasm forces into meiotic chromosomes. Telomeres or PCs (gold circle) connect to the NE through nucleoplasmic adaptors (schematized with a blue oval) and the nucleoplasmic domains (in green ovals) of SUN-domain proteins spanning the INM (in green; shown as a trimer). KASH domain proteins span the ONM (in red; shown as a trimer). Then SUN domains (in green helix) can interact with KASH domains (in red stub) in the PNS. Cytoplasmic adaptors (in purple) connect the cytoplasmic domains (in red ovals) of KASH proteins to the cytoskeleton (in black lines). The nucleoplasmic domains of SUN proteins can also interact with lamins (in orange). Cytoskeleton, cytoplasmic adaptors, SUN-KASH protein bridges, nucleoplasmic adaptors and telomeres/PCS form the central link that spans the nuclear envelope, transferring cytoplasm-derived forced into chromosomes. NE, nuclear envelope; INM, inner nuclear membrane; ONM, outer nuclear membrane; PNS, the perinuclear space.