PLK-1 promotes the merger of the parental genome into a single nucleus by triggering lamina disassembly.

Griselda Velez-Aguilera,Nicolas Tavernier,Jean-Marc Verbavatz,Sylvia Nkombo Nkoula,Lionel Pintard,Batool Ossareh-Nazari,Dimitra Paouneskou,Verena Jantsch,Nicolas Joly,Jana Link,Lucie Van Hove

doi:10.7554/elife.59510

Griselda Velez-Aguilera, Nicolas Tavernier + Show 9 more

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https://doi.org/10.7554/elife.59510

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Abstract

Life of sexually reproducing organisms starts with the fusion of the haploid egg and sperm gametes to form the genome of a new diploid organism. Using the newly fertilized Caenorhabditis elegans zygote, we show that the mitotic Polo-like kinase PLK-1 phosphorylates the lamin LMN-1 to promote timely lamina disassembly and subsequent merging of the parental genomes into a single nucleus after mitosis. Expression of non-phosphorylatable versions of LMN-1, which affect lamina depolymerization during mitosis, is sufficient to prevent the mixing of the parental chromosomes into a single nucleus in daughter cells. Finally, we recapitulate lamina depolymerization by PLK-1 in vitro demonstrating that LMN-1 is a direct PLK-1 target. Our findings indicate that the timely removal of lamin is essential for the merging of parental chromosomes at the beginning of life in C. elegans and possibly also in humans, where a defect in this process might be fatal for embryo development.

Highlights

After fertilization, the haploid gametes of the egg and sperm have to come together to form the genome of a new diploid organism
To determine if LMN-1 is a direct PLK-1 substrate in C. elegans, we tested whether PLK-1 directly phosphorylates LMN-1 in vitro
In C. elegans, the sperm brings in the centrosomes (Albertson, 1984), similar to the situation in humans and unlike the situation in mouse, where the first mitotic division is acentrosomal (Sathananthan et al, 1991) with parental chromosomes aligning on two separate mitotic spindles (Reichmann et al, 2018)

Summary

Introduction

The haploid gametes of the egg and sperm have to come together to form the genome of a new diploid organism. In the zygotes of humans, and in Caenorhabditis elegans, parental chromosomes are initially in separate pronuclei each surrounded by a nuclear envelope (NE) and meet for the first time during the first mitotic division. For this mitosis to occur properly, the NE of the pronuclei must be disassembled in a timely manner (Rahman et al, 2020). After rotation and centration of the nucleo-centrosomal complex, the NE breaks down in the vicinity of the centrosomes and between the juxtaposed pronuclei This allows the capture of the chromosomes by the microtubules and the mixing of the parental chromosomes (Figure 1—figure supplement 1A).

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