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RNA-on-X 1 and 2 in Drosophila melanogaster fulfill separate functions in dosage compensation
Umeå University, Faculty of Medicine, Department of Molecular Biology (Faculty of Medicine).
Umeå University, Faculty of Science and Technology, Department of Molecular Biology (Faculty of Science and Technology).
Umeå University, Faculty of Science and Technology, Department of Molecular Biology (Faculty of Science and Technology).ORCID iD: 0000-0003-4373-6790
2018 (English)In: PLoS Genetics, ISSN 1553-7390, E-ISSN 1553-7404, Vol. 14, no 12, article id e1007842Article in journal (Refereed) Published
Abstract [en]

In Drosophila melanogaster, the male-specific lethal (MSL) complex plays a key role in dosage compensation by stimulating expression of male X-chromosome genes. It consists of MSL proteins and two long noncoding RNAs, roX1 and roX2, that are required for spreading of the complex on the chromosome and are redundant in the sense that loss of either does not affect male viability. However, despite rapid evolution, both roX species are present in diverse Drosophilidae species, raising doubts about their full functional redundancy. Thus, we have investigated consequences of deleting roX1 and/or roX2 to probe their specific roles and redundancies in Dmelanogaster. We have created a new mutant allele of roX2 and show that roX1 and roX2 have partly separable functions in dosage compensation. In larvae, roX1 is the most abundant variant and the only variant present in the MSL complex when the complex is transmitted (physically associated with the X-chromosome) in mitosis. Loss of roX1 results in reduced expression of the genes on the X-chromosome, while loss of roX2 leads to MSL-independent upregulation of genes with male-biased testis-specific transcription. In roX1 roX2mutant, gene expression is strongly reduced in a manner that is not related to proximity to high-affinity sites. Our results suggest that high tolerance of mis-expression of the X-chromosome has evolved. We propose that this may be a common property of sex-chromosomes, that dosage compensation is a stochastic process and its precision for each individual gene is regulated by the density of high-affinity sites in the locus.

Place, publisher, year, edition, pages
Public Library Science , 2018. Vol. 14, no 12, article id e1007842
National Category
Genetics
Identifiers
URN: urn:nbn:se:umu:diva-155778DOI: 10.1371/journal.pgen.1007842ISI: 000455099000025PubMedID: 30532158OAI: oai:DiVA.org:umu-155778DiVA, id: diva2:1283037
Funder
Knut and Alice Wallenberg Foundation, 2014.0018Swedish Research Council, 2016-03306Swedish Cancer Society, CAN 2017/342Available from: 2019-01-28 Created: 2019-01-28 Last updated: 2019-01-28Bibliographically approved

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