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Distinct responses to rare codons in select Drosophila tissues

Scott R. Allen, Rebeccah K. Stewart, Michael Rogers, Ivan Jimenez Ruiz, Erez Cohen, View ORCID ProfileAlain Laederach, Christopher M. Counter, Jessica K. Sawyer, View ORCID ProfileDonald T. Fox
doi: https://doi.org/10.1101/2022.01.06.475284
Scott R. Allen
1Department of Cell Biology, Duke University Medical Center, Durham NC 27710, USA
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Rebeccah K. Stewart
2Department of Pharmacology & Cancer Biology, Duke University Medical Center, Durham NC 27710, USA
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Michael Rogers
2Department of Pharmacology & Cancer Biology, Duke University Medical Center, Durham NC 27710, USA
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Ivan Jimenez Ruiz
3Department of Biology, University of North Carolina, Chapel Hill NC 27599, USA
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Erez Cohen
1Department of Cell Biology, Duke University Medical Center, Durham NC 27710, USA
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Alain Laederach
3Department of Biology, University of North Carolina, Chapel Hill NC 27599, USA
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Christopher M. Counter
2Department of Pharmacology & Cancer Biology, Duke University Medical Center, Durham NC 27710, USA
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Jessica K. Sawyer
2Department of Pharmacology & Cancer Biology, Duke University Medical Center, Durham NC 27710, USA
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Donald T. Fox
1Department of Cell Biology, Duke University Medical Center, Durham NC 27710, USA
2Department of Pharmacology & Cancer Biology, Duke University Medical Center, Durham NC 27710, USA
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  • ORCID record for Donald T. Fox
  • For correspondence: don.fox@duke.edu
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ABSTRACT

Codon usage bias has long been appreciated to influence protein production. Yet, relatively few studies have analyzed the impacts of codon usage on tissue-specific mRNA and protein expression. Here, we use codon-modified reporters to perform an organism-wide screen in Drosophila melanogaster for distinct tissue responses to codon usage bias. These reporters reveal a cliff-like decline of protein expression near the limit of rare codon usage in endogenously expressed Drosophila genes. Near the edge of this limit, however, we find the testis and brain are uniquely capable of expressing rare codon-enriched reporters. We define a new metric of tissue-specific codon usage, the tissue-apparent Codon Adaptation Index, to reveal a conserved enrichment for rare codon usage in the endogenously expressed genes of both Drosophila and human testis. We further demonstrate a role for rare codons in restricting protein expression of an evolutionarily young gene, RpL10Aa, to the Drosophila testis. Rare codon-mediated restriction of this testis-specific protein is critical for female fertility. Our work highlights distinct responses to rarely used codons in select tissues, revealing a critical role for codon bias in tissue biology.

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. All rights reserved. No reuse allowed without permission.
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Posted January 06, 2022.
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Distinct responses to rare codons in select Drosophila tissues
Scott R. Allen, Rebeccah K. Stewart, Michael Rogers, Ivan Jimenez Ruiz, Erez Cohen, Alain Laederach, Christopher M. Counter, Jessica K. Sawyer, Donald T. Fox
bioRxiv 2022.01.06.475284; doi: https://doi.org/10.1101/2022.01.06.475284
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Distinct responses to rare codons in select Drosophila tissues
Scott R. Allen, Rebeccah K. Stewart, Michael Rogers, Ivan Jimenez Ruiz, Erez Cohen, Alain Laederach, Christopher M. Counter, Jessica K. Sawyer, Donald T. Fox
bioRxiv 2022.01.06.475284; doi: https://doi.org/10.1101/2022.01.06.475284

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