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Transcription factors drive opposite relationships between gene age and tissue specificity in male and female Drosophila gonads

View ORCID ProfileEvan Witt, View ORCID ProfileNicolas Svetec, View ORCID ProfileSigi Benjamin, View ORCID ProfileLi Zhao
doi: https://doi.org/10.1101/2020.12.09.418293
Evan Witt
Laboratory of Evolutionary Genetics and Genomics, The Rockefeller University, New York, NY 10065, USA
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Nicolas Svetec
Laboratory of Evolutionary Genetics and Genomics, The Rockefeller University, New York, NY 10065, USA
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Sigi Benjamin
Laboratory of Evolutionary Genetics and Genomics, The Rockefeller University, New York, NY 10065, USA
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Li Zhao
Laboratory of Evolutionary Genetics and Genomics, The Rockefeller University, New York, NY 10065, USA
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  • For correspondence: lzhao@rockefeller.edu
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Abstract

Evolutionarily young genes are usually preferentially expressed in the testis across species. While it is known that older genes are generally more broadly expressed than younger genes, the properties that shaped this pattern are unknown. Older genes may gain expression across other tissues uniformly, or faster in certain tissues than others. Using Drosophila gene expression data, we confirmed previous findings that younger genes are disproportionately testis-biased and older genes are disproportionately ovary-biased. We found that the relationship between gene age and expression is stronger in the ovary than any other tissue, and weakest in testis. We performed ATAC-seq on Drosophila testis and found that while genes of all ages are more likely to have open promoter chromatin in testis than in ovary, promoter chromatin alone does not explain the ovary-bias of older genes. Instead, we found that upstream transcription factor (TF) expression is highly predictive of gene expression in ovary, but not in testis. In ovary, TF expression is more predictive of gene expression than open promoter chromatin, whereas testis gene expression is similarly influenced by both TF expression and open promoter chromatin. We propose that the testis is uniquely able to expresses younger genes controlled by relatively few TFs, while older genes with more TF partners are broadly expressed with peak expression most likely in ovary. The testis allows widespread baseline expression that is relatively unresponsive to regulatory changes, whereas the ovary transcriptome is more responsive to trans-regulation and has a higher ceiling for gene expression.

Competing Interest Statement

The authors have declared no competing interest.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC 4.0 International license.
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Posted January 13, 2021.
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Transcription factors drive opposite relationships between gene age and tissue specificity in male and female Drosophila gonads
Evan Witt, Nicolas Svetec, Sigi Benjamin, Li Zhao
bioRxiv 2020.12.09.418293; doi: https://doi.org/10.1101/2020.12.09.418293
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Transcription factors drive opposite relationships between gene age and tissue specificity in male and female Drosophila gonads
Evan Witt, Nicolas Svetec, Sigi Benjamin, Li Zhao
bioRxiv 2020.12.09.418293; doi: https://doi.org/10.1101/2020.12.09.418293

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