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Reference - PMID:30089908 - Gamete fusion triggers bipartite transcription factor assembly to block re-fertilization.

Reference summary

PubMed ID
PMID:30089908
Title
Gamete fusion triggers bipartite transcription factor assembly to block re-fertilization.
Authors
Vještica A, Merlini L, Nkosi PJ, Martin SG
Citation
Nature 2018 Aug;560(7718):397-400
Publication year
2018
Abstract
The ploidy cycle, which is integral to sexual reproduction, requires meiosis to halve chromosome numbers as well as mechanisms that ensure zygotes are formed by exactly two partners 1-4 . During sexual reproduction of the fungal model organism Schizosaccharomyces pombe, haploid P and M cells fuse to form a diploid zygote that immediately enters meiosis 5 . Here we reveal that rapid post-fusion reconstitution of a bipartite transcription factor blocks re-fertilization. We first identify mutants that undergo transient cell fusion involving cytosol exchange but not karyogamy, and show that this drives distinct cell fates in the two gametes. The P partner undergoes lethal haploid meiosis, whereas the M cell persists in mating. The zygotic transcription that drives meiosis is rapidly initiated first from the P parental genome, even in wild-type cells. This asymmetric gene expression depends on a bipartite complex formed post-fusion between the cytosolic M-cell-specific peptide Mi and the nuclear P-cell-specific homeobox protein Pi 6,7 , which captures Mi in the P nucleus. Zygotic transcription is thus poised to initiate in the P nucleus as fast as Mi reaches it after fusion, a design that we reconstruct using two synthetic interactors localized to the nucleus and the cytosol of two respective partner cells. Notably, delaying zygotic transcription-by postponing Mi expression or deleting its transcriptional target in the P genome-leads to zygotes fusing with additional gametes, thus forming polyploids and eventually aneuploid progeny. The signalling cascade to block re-fertilization shares components with, but bifurcates from, meiotic induction 8-10 . Thus, a cytoplasmic connection upon gamete fusion leads to asymmetric reconstitution of a bipartite transcription factor to rapidly block re-fertilization and induce meiosis, ensuring genome maintenance during sexual reproduction.

Annotation

GO biological process

GO:0051728 - cell cycle switching, mitotic to meiotic cell cycle

Genes:

GO:0000755 - cytogamy

Genes:

GO:0140538 - negative regulation of conjugation with zygote

Genes:

GO:0034504 - protein localization to nucleus

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GO cellular component

GO:0000785 - chromatin

Genes:

GO:0005737 - cytoplasm

Genes:

GO:0005634 - nucleus

Genes:

GO:0062071 - Pi Mi complex

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GO molecular function

GO:0001228 - DNA-binding transcription activator activity, RNA polymerase II-specific

Genes:

GO:0005515 - protein binding

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Multi-locus phenotype

FYPO:0006669 - abnormal mating between three cells

Genes:

Genotypes:

FYPO:0003363 - abolished cytogamy

Genes:

Genotypes:

FYPO:0001886 - meiotic cell cycle entry and sporulation in haploid

Genes:

Genotypes:

FYPO:0006014 - promiscuous mating

Genes:

Genotypes:

Single locus phenotype

FYPO:0006669 - abnormal mating between three cells

Genes:

Genotypes:

FYPO:0000413 - abolished cell fusion during mating

Genes:

Genotypes:

FYPO:0006349 - abolished protein localization to chromatin at promoter

Genes:

Genotypes:

FYPO:0006685 - abolished protein localization to mating partner nucleus in zygote

Genes:

Genotypes:

FYPO:0006674 - abolished protein localization to nucleus during mating

Genes:

Genotypes:

FYPO:0006673 - decreased DNA content in spore

Genes:

Genotypes:

FYPO:0004807 - narrow cell fusion site following mating

Genes:

Genotypes:

FYPO:0003797 - normal conjugation frequency

Genes:

Genotypes:

FYPO:0001147 - normal mating efficiency

Genes:

Genotypes:

FYPO:0000590 - normal sporulation

Genes:

Genotypes:

FYPO:0002052 - normal sporulation frequency

Genes:

Genotypes:

FYPO:0006014 - promiscuous mating

Genes:

Genotypes:

FYPO:0001983 - protein absent from cell

Genes:

Genotypes:

FYPO:0006672 - transient cell fusion during mating followed by meiotic cell cycle entry and sporulation

Genes:

Genotypes:

FYPO:0000678 - unequal homologous chromosome segregation

Genes:

Genotypes: