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.

Tethering of Telomeres to the Nuclear Envelope Is Mediated by SUN1-MAJIN and Possibly Promoted by SPDYA-CDK2 During Meiosis

“…During meiosis, telomeres are tethered to the NE. This tethering is critical for meiotic chromosome alignment and synaptic pairing of the homologs (Harper et al, 2004;Lee et al, 2015;Zeng et al, 2017). Many proteins are involved in this tethering process, such as the LINC (linker of nucleoskeleton and cytoskeleton) complex, the "adaptor, " and the shelterin complex (Shibuya et al, 2015;Burke, 2018;Li and Liu, 2020).…”

Parental genome unification is highly erroneous in mammalian embryos

“…The perinuclear microtubules that wrapped around the nuclear envelope appeared to be in a suitable arrangement for mediating chromosome transport towards centrosomes, as they covered most of the pronuclear surfaces and were highly enriched at the pronuclear interface, where at least one of the centrosomes was located ( Figure 4D). Adapters in the nuclear envelope can link chromosomes to microtubules and thereby transduce forces across the nuclear envelope (Zeng et al, 2018). Transport towards centrosomes in interphase is typically mediated by the minus-end directed motor protein dynein (Malone et al, 2003;Quintyne et al, 1999).…”

“…The dynein-dependent movement of chromosomes toward the centrosome in zygotes is reminiscent of the mechanisms involved in forming telomere bouquets established in the early stages of meiosis (Zeng et al, 2018). The telomeres cluster in proximity to the centrosome in preparation for meiotic recombination (Sato et al, 2009;Shibuya et al, 2014).…”

The nuclear envelope in higher plant mitosis and meiosis

“…In plants, the molecular mechanisms involved in the regulation of meiotic LINC complex function may be different. Furthermore, how telomeres are connected to the LINC complexes during plant meiosis is entirely unclear, because meiosisspecific adaptor proteins or factors that interact with SUN proteins in a meiosis-dependent manner have not been further identified [96]. In addition, many of the essential proteins involved in telomere organization do not have orthologous genes in the plant kingdom.…”