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Adaptation of codon and amino acid use for translational functions in highly expressed cricket genes

View ORCID ProfileCarrie A. Whittle, View ORCID ProfileArpita Kulkarni, View ORCID ProfileNina Chung, View ORCID ProfileCassandra G. Extavour
doi: https://doi.org/10.1101/2020.08.31.276477
Carrie A. Whittle
1Department of Organismic and Evolutionary Biology, Harvard University, 16 Divinity Avenue, Cambridge MA 02138, USA
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Arpita Kulkarni
1Department of Organismic and Evolutionary Biology, Harvard University, 16 Divinity Avenue, Cambridge MA 02138, USA
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Nina Chung
1Department of Organismic and Evolutionary Biology, Harvard University, 16 Divinity Avenue, Cambridge MA 02138, USA
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Cassandra G. Extavour
1Department of Organismic and Evolutionary Biology, Harvard University, 16 Divinity Avenue, Cambridge MA 02138, USA
2Department of Molecular and Cellular Biology, Harvard University, 16 Divinity Avenue, Cambridge MA
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  • For correspondence: extavour@oeb.harvard.edu
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Abstract

Background For multicellular organisms, much remains unknown about the dynamics of synonymous codon and amino acid use in highly expressed genes, including whether their use varies with expression in different tissue types and sexes. Moreover, specific codons and amino acids may have translational functions in highly transcribed genes, that largely depend on their relationships to tRNA gene copies in the genome. However, these relationships and putative functions are poorly understood, particularly in multicellular systems.

Results Here, we rigorously studied codon and amino acid use in highly expressed genes from reproductive and nervous system tissues (male and female gonad, somatic reproductive system, brain, ventral nerve cord, and male accessory glands) in the cricket Gryllus bimaculatus. We report an optimal codon, defined as the codon preferentially used in highly expressed genes, for each of the 18 amino acids with synonymous codons in this organism. The optimal codons were largely shaped by selection, and their identities were mostly shared among tissue types and both sexes. However, the frequency of optimal codons was highest in gonadal genes. Concordant with translational selection, a majority of the optimal codons had abundant matching tRNA gene copies in the genome, but sometimes obligately required wobble tRNAs. We suggest the latter may comprise a mechanism for slowing translation of abundant transcripts, particularly for cell-cycle genes. Non-optimal codons, defined as those least commonly used in highly transcribed genes, intriguingly often had abundant tRNAs, and had elevated use in a subset of genes with specialized functions (gametic and apoptosis genes), suggesting their use promotes the upregulation of particular mRNAs. In terms of amino acids, we found evidence suggesting that amino acid frequency, tRNA gene copy number, and amino acid biosynthetic costs (size/complexity) had all interdependently evolved in this insect model, potentially for translational optimization.

Conclusions Collectively, the results strongly suggest that codon use in highly expressed genes, including optimal, wobble, and non-optimal codons, and their tRNAs abundances, as well as amino acid use, have been adapted for various functional roles in translation within this cricket. The effects of expression in different tissue types and the two sexes are discussed.

Competing Interest Statement

The authors have declared no competing interest.

  • List of abbreviations

    Top5One-tissue
    genes with an expression level in the top 5% in one tissue type only, and not in the other eight tissues
    FPKM
    frequency per kilobase million
    MWU-test
    Mann-Whitney U-test
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    Posted September 01, 2020.
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    Adaptation of codon and amino acid use for translational functions in highly expressed cricket genes
    Carrie A. Whittle, Arpita Kulkarni, Nina Chung, Cassandra G. Extavour
    bioRxiv 2020.08.31.276477; doi: https://doi.org/10.1101/2020.08.31.276477
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    Adaptation of codon and amino acid use for translational functions in highly expressed cricket genes
    Carrie A. Whittle, Arpita Kulkarni, Nina Chung, Cassandra G. Extavour
    bioRxiv 2020.08.31.276477; doi: https://doi.org/10.1101/2020.08.31.276477

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