Early developmental, meiosis-specific proteins - Spo11, Msh4-1, and Msh5 - Affect subsequent genome reorganization in Paramecium tetraurelia

Iwona Rzeszutek; Estienne C Swart; Sylwia Pabian-Jewuła; Antonietta Russo; Mariusz Nowacki

doi:10.1016/j.bbamcr.2022.119239

Early developmental, meiosis-specific proteins - Spo11, Msh4-1, and Msh5 - Affect subsequent genome reorganization in Paramecium tetraurelia

Biochim Biophys Acta Mol Cell Res. 2022 Jun;1869(6):119239. doi: 10.1016/j.bbamcr.2022.119239. Epub 2022 Feb 15.

Authors

Iwona Rzeszutek¹, Estienne C Swart², Sylwia Pabian-Jewuła³, Antonietta Russo⁴, Mariusz Nowacki⁵

Affiliations

¹ Institute of Cell Biology, University of Bern, Baltzerstrasse 4, 3012 Bern, Switzerland; Graduate School for Cellular and Biomedical Sciences, University of Bern, Freiestrasse 1, 3012 Bern, Switzerland; Institute of Biology and Biotechnology, Department of Biotechnology, University of Rzeszow, Pigonia 1, 35-310 Rzeszow, Poland.
² Institute of Cell Biology, University of Bern, Baltzerstrasse 4, 3012 Bern, Switzerland; Max Planck Institute for Developmental Biology, Max-Planck-Ring 5, 72076 Tuebingen, Germany.
³ Institute of Cell Biology, University of Bern, Baltzerstrasse 4, 3012 Bern, Switzerland; Centre of Postgraduate Medical Education, Department of Clinical Cytology, Marymoncka 99/103, 01-813 Warsaw, Poland.
⁴ Institute of Cell Biology, University of Bern, Baltzerstrasse 4, 3012 Bern, Switzerland; Medical Biochemistry and Molecular Biology Department, UKS, Saarland Medical Center, Kirrberger Str. 100, 66421 Homburg, Germany.
⁵ Institute of Cell Biology, University of Bern, Baltzerstrasse 4, 3012 Bern, Switzerland. Electronic address: mariusz.nowacki@izb.unibe.ch.

PMID: 35181406
DOI: 10.1016/j.bbamcr.2022.119239

Abstract

Developmental DNA elimination in Paramecium tetraurelia occurs through a trans-nuclear comparison of the genomes of two distinct types of nuclei: the germline micronucleus (MIC) and the somatic macronucleus (MAC). During sexual reproduction, which starts with meiosis of the germline nuclei, MIC-limited sequences including Internal Eliminated Sequences (IESs) and transposons are eliminated from the developing MAC in a process guided by noncoding RNAs (scnRNAs and iesRNAs). However, our current understanding of this mechanism is still very limited. Therefore, studying both genetic and epigenetic aspects of these processes is a crucial step to understand this phenomenon in more detail. Here, we describe the involvement of homologs of classical meiotic proteins, Spo11, Msh4-1, and Msh5 in this phenomenon. Based on our analyses, we propose that proper functioning of Spo11, Msh4-1, and Msh5 during Paramecium sexual reproduction are necessary for genome reorganization and viable progeny. Also, we show that double-strand breaks (DSBs) in DNA induced during meiosis by Spo11 are crucial for proper IESs excision. In summary, our investigations show that early sexual reproduction processes may significantly influence later somatic genome integrity.

Keywords: Genome rearrangement; Meiosis; Msh4; Msh5; Paramecium; Spo11.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Germ Cells
Macronucleus / genetics
Macronucleus / metabolism
Meiosis / genetics
Paramecium tetraurelia* / genetics
Paramecium tetraurelia* / metabolism
RNA, Untranslated / metabolism

Substances

RNA, Untranslated