27nt-RNAs guide histone variant deposition via 'RNA-induced DNA replication interference' and thus transmit parental genome partitioning in Stylonychia

During sexual reproduction in the unicellular ciliate Stylonychia somatic macronuclei differentiate from germline micronuclei. Thereby, programmed sequence reduction takes place, leading to the elimination of > 95% of germline sequences, which priorly adopt heterochromatin structure via H3K27me3....

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Bibliographic Details
Published in:Epigenetics & chromatin 2018-06, Vol.11 (1), p.31-31, Article 31
Main Authors: Postberg, Jan, Jönsson, Franziska, Weil, Patrick Philipp, Bulic, Aneta, Juranek, Stefan Andreas, Lipps, Hans-Joachim
Format: Article
Language:English
Subjects:
Argonaute Proteins - metabolism
Chromosomes
Ciliates
Ciliophora - genetics
Ciliophora - physiology
Deoxyribonucleic acid
DNA
DNA biosynthesis
DNA methylation
DNA Replication
Gene expression
Genetic aspects
Genetic Variation
Genome, Protozoan
Genomes
Heterochromatin
Histone H3
Histones
Histones - genetics
Kinases
Macronuclei
Micronuclei
Micronucleus, Germline - genetics
Nucleosomes
Nucleotide sequence
Oxytricha
Polytene
Proteins
Replication
Ribonucleic acid
RNA
RNA, Guide, CRISPR-Cas Systems
RNA, Protozoan - genetics
RNA-mediated interference
Sexual reproduction
Stylonychia
Tetrahymena
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Summary:During sexual reproduction in the unicellular ciliate Stylonychia somatic macronuclei differentiate from germline micronuclei. Thereby, programmed sequence reduction takes place, leading to the elimination of > 95% of germline sequences, which priorly adopt heterochromatin structure via H3K27me3. Simultaneously, 27nt-ncRNAs become synthesized from parental transcripts and are bound by the Argonaute protein PIWI1. These 27nt-ncRNAs cover sequences destined to the developing macronucleus and are thought to protect them from degradation. We provide evidence and propose that RNA/DNA base-pairing guides PIWI1/27nt-RNA complexes to complementary macronucleus-destined DNA target sequences, hence transiently causing locally stalled replication during polytene chromosome formation. This spatiotemporal delay enables the selective deposition of temporarily available histone H3.4K27me3 nucleosomes at all other sequences being continuously replicated, thus dictating their prospective heterochromatin structure before becoming developmentally eliminated. Concomitantly, 27nt-RNA-covered sites remain protected. We introduce the concept of 'RNA-induced DNA replication interference' and explain how the parental functional genome partition could become transmitted to the progeny.
ISSN:1756-8935
1756-8935
DOI:10.1186/s13072-018-0201-5