Relocation Facilitates the Acquisition of Short Cis-Regulatory Regions that Drive the Expression of Retrogenes during Spermatogenesis in Drosophila

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dc.authorid0000-0002-5298-6997
dc.authorid0000-0002-4742-7963
dc.authorwosidÖzdil, Fulya/ABA-4197-2020
dc.contributor.authorSorourian, Mehran
dc.contributor.authorKunte, Mansi M.
dc.contributor.authorDomingues, Susana
dc.contributor.authorGallach, Miguel
dc.contributor.authorÖzdil, Fulya
dc.contributor.authorRio, Javier
dc.contributor.authorBetran, Esther
dc.date.accessioned2022-05-11T14:45:23Z
dc.date.available2022-05-11T14:45:23Z
dc.date.issued2014
dc.departmentFakülteler, Ziraat Fakültesi, Tarımsal Biyoteknoloji Bölümü
dc.description.abstractRetrogenes are functional processed copies of genes that originate via the retrotranscription of an mRNA intermediate and often exhibit testis-specific expression. Although this expression pattern appears to be favored by selection, the origin of such expression bias remains unexplained. Here, we study the regulation of two young testis-specific Drosophila retrogenes, Dntf-2r and Pros28.1A, using genetic transformation and the enhanced green fluorescent protein reporter gene in Drosophila melanogaster. We show that two different short (< 24 bp) regions upstream of the transcription start sites (TSSs) act as testis-specific regulatory motifs in these genes. The Dntf-2r regulatory region is similar to the known beta 2 tubulin 14-bp testis motif (beta 2-tubulin gene upstream element 1 [beta 2-UE1]). Comparative sequence analyses reveal that this motif was already present before the Dntf-2r insertion and was likely driving the transcription of a noncoding RNA. We also show that the beta 2-UE1 occurs in the regulatory regions of other testis-specific retrogenes, and is functional in either orientation. In contrast, the Pros28.1A testes regulatory region in D. melanogaster appears to be novel. Only Pros28.1B, an older paralog of the Pros28.1 gene family, seems to carry a similar regulatory sequence. It is unclear how the Pros28.1A regulatory region was acquired in D. melanogaster, but it might have evolved de novo from within a region that may have been preprimed for testes expression. We conclude that relocation is critical for the evolutionary origin of male germline-specific cis-regulatory regions of retrogenes because expression depends on either the site of the retrogene insertion or the sequence changes close to the TSS thereafter. As a consequence we infer that positive selection will play a role in the evolution of these regulatory regions and can often act from the moment of the retrocopy insertion.
dc.description.sponsorshipNational Institute of General Medical Sciences of the National Institutes of HealthUnited States Department of Health & Human ServicesNational Institutes of Health (NIH) - USANIH National Institute of General Medical Sciences (NIGMS) [R01GM071813]; ARRA; UT; NATIONAL INSTITUTE OF GENERAL MEDICAL SCIENCESUnited States Department of Health & Human ServicesNational Institutes of Health (NIH) - USANIH National Institute of General Medical Sciences (NIGMS) [R01GM071813] Funding Source: NIH RePORTER
dc.description.sponsorshipThe authors thank J. Coyne, P. Gibert, F. Lemeunier, M. Long, M.-L. Wu, C.-I. Wu, and the UC San Diego Drosophila Stock Center for providing wild-type Drosophila strains used in this work and Genetic Services, Inc. and the Bloomington Drosophila Stock Center at Indiana University for providing the mutant stocks used in this study. They also thank H. White-Cooper for providing them with her in situ hybridization protocol before publication and for all her advice on its implementation in their lab. They want to thank four anonymous reviewers for comments on this work. M. G. wants to thank Arndt von Haeseler for his support when finalizing the manuscript. This work was supported by, the National Institute of General Medical Sciences of the National Institutes of Health under award number R01GM071813, an ARRA Supplement and UT Arlington startup funds to E. B. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health.
dc.identifier.doi10.1093/molbev/msu168
dc.identifier.endpage2180
dc.identifier.issn0737-4038
dc.identifier.issn1537-1719
dc.identifier.issue8en_US
dc.identifier.pmid24855141
dc.identifier.startpage2170
dc.identifier.urihttps://doi.org/10.1093/molbev/msu168
dc.identifier.urihttps://hdl.handle.net/20.500.11776/10027
dc.identifier.volume31
dc.identifier.wosWOS:000339927800017
dc.identifier.wosqualityQ1
dc.indekslendigikaynakWeb of Science
dc.indekslendigikaynakPubMed
dc.institutionauthorGallach, Miguel
dc.language.isoen
dc.publisherOxford Univ Press
dc.relation.ispartofMolecular Biology and Evolution
dc.relation.publicationcategoryMakale - Uluslararası Hakemli Dergi - Kurum Öğretim Elemanıen_US
dc.rightsinfo:eu-repo/semantics/openAccess
dc.subjectDrosophila
dc.subjectretrogene
dc.subjecttestis expression
dc.subjectregulatory element
dc.subjectgene duplication
dc.subjectgene relocation
dc.subjectMolecular Evolution
dc.subjectTranscriptional Regulation
dc.subjectComparative Genomics
dc.subjectGene-Expression
dc.subjectRetroposed Gene
dc.subjectOrigin
dc.subjectChromosome
dc.subjectSelection
dc.subjectMovement
dc.subjectJingwei
dc.titleRelocation Facilitates the Acquisition of Short Cis-Regulatory Regions that Drive the Expression of Retrogenes during Spermatogenesis in Drosophila
dc.typeArticle

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