Paralog transcriptional differentiation in the D. melanogaster-specific gene family Sdic across populations and spermatogenesis stages

Abstract How recently originated gene copies become stable genomic components remains uncertain as high sequence similarity of young duplicates precludes their functional characterization. The tandem multigene family Sdic is specific to Drosophila melanogaster and has been annotated across multiple...

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Main Authors: Bryan D. Clifton, Imtiyaz Hariyani, Ashlyn Kimura, Fangning Luo, Alvin Nguyen, José M. Ranz
Format: Article
Language:English
Published: Nature Portfolio 2023-10-01
Series:Communications Biology
Online Access:https://doi.org/10.1038/s42003-023-05427-4
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author Bryan D. Clifton
Imtiyaz Hariyani
Ashlyn Kimura
Fangning Luo
Alvin Nguyen
José M. Ranz
author_facet Bryan D. Clifton
Imtiyaz Hariyani
Ashlyn Kimura
Fangning Luo
Alvin Nguyen
José M. Ranz
author_sort Bryan D. Clifton
collection DOAJ
description Abstract How recently originated gene copies become stable genomic components remains uncertain as high sequence similarity of young duplicates precludes their functional characterization. The tandem multigene family Sdic is specific to Drosophila melanogaster and has been annotated across multiple reference-quality genome assemblies. Here we show the existence of a positive correlation between Sdic copy number and total expression, plus vast intrastrain differences in mRNA abundance among paralogs, using RNA-sequencing from testis of four strains with variable paralog composition. Single cell and nucleus RNA-sequencing data expose paralog expression differentiation in meiotic cell types within testis from third instar larva and adults. Additional RNA-sequencing across synthetic strains only differing in their Y chromosomes reveal a tissue-dependent trans-regulatory effect on Sdic: upregulation in testis and downregulation in male accessory gland. By leveraging paralog-specific expression information from tissue- and cell-specific data, our results elucidate the intraspecific functional diversification of a recently expanded tandem gene family.
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spelling doaj.art-4183d60dc9c841918025408c1a6175062023-11-20T10:33:52ZengNature PortfolioCommunications Biology2399-36422023-10-016111110.1038/s42003-023-05427-4Paralog transcriptional differentiation in the D. melanogaster-specific gene family Sdic across populations and spermatogenesis stagesBryan D. Clifton0Imtiyaz Hariyani1Ashlyn Kimura2Fangning Luo3Alvin Nguyen4José M. Ranz5Department of Ecology and Evolutionary Biology, University of California IrvineDepartment of Ecology and Evolutionary Biology, University of California IrvineDepartment of Ecology and Evolutionary Biology, University of California IrvineDepartment of Ecology and Evolutionary Biology, University of California IrvineDepartment of Ecology and Evolutionary Biology, University of California IrvineDepartment of Ecology and Evolutionary Biology, University of California IrvineAbstract How recently originated gene copies become stable genomic components remains uncertain as high sequence similarity of young duplicates precludes their functional characterization. The tandem multigene family Sdic is specific to Drosophila melanogaster and has been annotated across multiple reference-quality genome assemblies. Here we show the existence of a positive correlation between Sdic copy number and total expression, plus vast intrastrain differences in mRNA abundance among paralogs, using RNA-sequencing from testis of four strains with variable paralog composition. Single cell and nucleus RNA-sequencing data expose paralog expression differentiation in meiotic cell types within testis from third instar larva and adults. Additional RNA-sequencing across synthetic strains only differing in their Y chromosomes reveal a tissue-dependent trans-regulatory effect on Sdic: upregulation in testis and downregulation in male accessory gland. By leveraging paralog-specific expression information from tissue- and cell-specific data, our results elucidate the intraspecific functional diversification of a recently expanded tandem gene family.https://doi.org/10.1038/s42003-023-05427-4
spellingShingle Bryan D. Clifton
Imtiyaz Hariyani
Ashlyn Kimura
Fangning Luo
Alvin Nguyen
José M. Ranz
Paralog transcriptional differentiation in the D. melanogaster-specific gene family Sdic across populations and spermatogenesis stages
Communications Biology
title Paralog transcriptional differentiation in the D. melanogaster-specific gene family Sdic across populations and spermatogenesis stages
title_full Paralog transcriptional differentiation in the D. melanogaster-specific gene family Sdic across populations and spermatogenesis stages
title_fullStr Paralog transcriptional differentiation in the D. melanogaster-specific gene family Sdic across populations and spermatogenesis stages
title_full_unstemmed Paralog transcriptional differentiation in the D. melanogaster-specific gene family Sdic across populations and spermatogenesis stages
title_short Paralog transcriptional differentiation in the D. melanogaster-specific gene family Sdic across populations and spermatogenesis stages
title_sort paralog transcriptional differentiation in the d melanogaster specific gene family sdic across populations and spermatogenesis stages
url https://doi.org/10.1038/s42003-023-05427-4
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