Abstract

BackgroundMeiosis is essential for sexual reproduction and generates genetically diverse haploid gametes from a diploid germ cell. Reduction of ploidy depends on active chromosome movements during early meiotic prophase I. Chromosome movements require telomere attachment to the nuclear envelope. This attachment is mediated by telomere adaptor proteins. Telomere adaptor proteins have to date been identified in fission yeast and mice. In the mouse, they form a complex composed of the meiotic proteins TERB1, TERB2, and MAJIN. No sequence similarity was observed between these three mouse proteins and the adaptor proteins of fission yeast, raising the question of the evolutionary history and significance of this specific protein complex.ResultHere, we show the TERB1, TERB2, and MAJIN proteins are found throughout the Metazoa and even in early-branching non-bilateral phyla such as Cnidaria, Placozoa and Porifera. Metazoan TERB1, TERB2, and MAJIN showed comparable domain architecture across all clades. Furthermore, the protein domains involved in the formation of the complex as well as those involved for the interaction with the telomere shelterin protein and the LINC complexes revealed high sequence similarity. Finally, gene expression in the cnidarian Hydra vulgaris provided evidence that the TERB1-TERB2-MAJIN complex is selectively expressed in the germ line.ConclusionOur results indicate that the TERB1-TERB2-MAJIN complex has an ancient origin in metazoans, suggesting conservation of meiotic functions.

Highlights

  • Meiosis is essential for sexual reproduction and generates genetically diverse haploid gametes from a diploid germ cell

  • Our results indicate that the Telomere repeat binding bouquet (TERB1)-TERB2-Membrane anchored junction protein (MAJIN) complex has an ancient origin in metazoans, suggesting conservation of meiotic functions

  • TERB1, TERB2, and MAJIN are ancestral metazoans proteins To identify candidate TERB1, TERB2 and MAJIN homologs in other taxa, we carried out a bioinformatic screen of public sequence databases using PSI-BLAST [30]

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Summary

Introduction

Meiosis is essential for sexual reproduction and generates genetically diverse haploid gametes from a diploid germ cell. Telomere adaptor proteins have to date been identified in fission yeast and mice In the mouse, they form a complex composed of the meiotic proteins TERB1, TERB2, and MAJIN. The forces required for meiotic chromosome movements are generated in the cytoplasm and transduced into the nucleus via LINC (Linker of Nucleoskeleton and Cytoskeleton) complexes of the nuclear envelope (NE) [3,4,5,6] In mice, this complex is composed of the transmembrane proteins SUN1 and SUN2 of the inner nuclear membrane (INM), and the KASH5 protein in the outer nuclear membrane (ONM) [7,8,9,10,11]. MAJIN possesses DNA binding properties and is anchored to the INM via a transmembrane helix at its C-terminus [13, 14, 19] (Fig. 1a)

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