Bisection of the X chromosome disrupts the initiation of chromosome silencing during meiosis in Caenorhabditis elegans

Yisrael Rappaport, Hanna Achache, Roni Falk, Omer Murik, Oren Ram, Yonatan B. Tzur*

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

4 Scopus citations

Abstract

During meiosis, gene expression is silenced in aberrantly unsynapsed chromatin and in heterogametic sex chromosomes. Initiation of sex chromosome silencing is disrupted in meiocytes with sex chromosome-autosome translocations. To determine whether this is due to aberrant synapsis or loss of continuity of sex chromosomes, we engineered Caenorhabditis elegans nematodes with non-translocated, bisected X chromosomes. In early meiocytes of mutant males and hermaphrodites, X segments are enriched with euchromatin assembly markers and active RNA polymerase II staining, indicating active transcription. Analysis of RNA-seq data showed that genes from the X chromosome are upregulated in gonads of mutant worms. Contrary to previous models, which predicted that any unsynapsed chromatin is silenced during meiosis, our data indicate that unsynapsed X segments are transcribed. Therefore, our results suggest that sex chromosome chromatin has a unique character that facilitates its meiotic expression when its continuity is lost, regardless of whether or not it is synapsed.

Original languageAmerican English
Article number4802
JournalNature Communications
Volume12
Issue number1
DOIs
StatePublished - 10 Aug 2021

Bibliographical note

Funding Information:
We thank the Caenorhabditis Genetics Center for kindly providing strains. We thank Abby Dernburg for the anti-HIM-8 antibody and Sarit Smolikove for the anti-SYP-4 and anti-SYP-1 antibodies. We thank Y. Yarden and E. Meshorer for sharing reagents, and B. Schumacher for helpful discussions. We thank Yuval Nevo and the team at the Info-CORE, Bioinformatics Unit of the I-CORE Computation Center, The Hebrew University and Hadassah Medical Center, Jerusalem, Israel, for the differential expression analysis, Michal Bronstein and the team at the Center for Genomic Technologies of the Alexander Silberman Life Sciences Institute for their help with Nanopore sequencing, and Michael Gershovis and the team of Israel National Center for Personalized Medicine for their help in Illumina DNA genomic sequencing. This work was supported by the European Research Council (ERC, #715260 SC-EpiCode), the Israeli Center of Research Excellence (I-CORE) program, the Israel Science Foundation (ISF, #1618/16), and Azrieli Foundation Scholar Program for Distinguished Junior Faculty to O.R. and by the Israel Science Foundation (grants #1283/15 and #2090/15) and by the Ministry of Science & Technology, Israel (#100594) to Y.B.T.

Publisher Copyright:
© 2021, The Author(s).

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