The Transmembrane Protein Semi1 Positions Gamete Nuclei for Reciprocal Fertilization in Tetrahymena.

Takahiko Akematsu,Felix Kosta,Josef Loidl,Elisabeth Holzer,Rosalía Sánchez-Fernández

doi:10.1016/j.isci.2019.100749

Abstract

SummaryDuring sexual reproduction in the ciliate, Tetrahymena thermophila, cells of complementary mating type pair (“conjugate”) undergo simultaneous meiosis and fertilize each other. In both mating partners only one of the four meiotic products is “selected” to escape autophagy, and this nucleus divides mitotically to produce two pronuclei. The migrating pronucleus of one cell translocates to the mating partner and fuses with its stationary pronucleus and vice versa. Selection of the designated gametic nucleus was thought to depend on its position within the cell because it always attaches to the junction with the partner cell. Here we show that a transmembrane protein, Semi1, is crucial for attachment. Loss of Semi1 causes failure to attach and consequent infertility. However, a nucleus is selected and gives rise to pronuclei regardless of Semi1 expression, indicating that attachment of a nucleus to the junction is not a precondition for selection but follows the selection process.

Highlights

The model ciliate Tetrahymena thermophila stably maintains different germline and somatic genomes in two separate nuclei within a single cytoplasm
One of the pronuclei migrates to the partner cell to fertilize its stationary pronucleus, whereas the other becomes fertilized by the migratory pronucleus of the partner cell
Attenuated post-meiotic DNA double-strand break (PM-DSB) formation culminates in autophagy for all haploid MICs (hMICs) (Akematsu et al, 2017), strongly suggesting that hMIC selection involves self-inflicted DNA damage in all hMICs followed by DNA repair in only one

Summary

Introduction

The model ciliate Tetrahymena thermophila stably maintains different germline and somatic genomes in two separate nuclei within a single cytoplasm. The gH2AX foci disappear only from one hMIC, and this occurs at the same time as histone H3 becomes acetylated at lysine 56 (H3K56ac), which is an epigenetic marker of reconstituted chromatin on nascent DNA (Shi and Oberdoerffer, 2012; Chen et al, 2008). This hMIC undergoes another round of mitosis, known as gametogenic mitosis, to produce gametic pronuclei (Akematsu et al, 2017). The DNA repair proteins DNAPKcs (involved in DNA repair by non-homologous end-joining) and Rad (involved in recombinational repair) and the histone H3-H4 chaperone Asf localize to the selected hMIC (Akematsu et al, 2017)

Methods

Results

Discussion

Conclusion