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Relaxed sequence constraints favor mutational freedom in idiosyncratic metazoan mitochondrial tRNAs

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  • Bernhard Kuhle

    (The Skaggs Institute for Chemical Biology, Scripps Research
    The Scripps Research Institute
    The Scripps Research Institute)

  • Joseph Chihade

    (Carleton College)

  • Paul Schimmel

    (The Skaggs Institute for Chemical Biology, Scripps Research
    The Scripps Research Institute
    The Scripps Research Institute
    The Scripps Florida Research Institute)

Abstract

Metazoan complexity and life-style depend on the bioenergetic potential of mitochondria. However, higher aerobic activity and genetic drift impose strong mutation pressure and risk of irreversible fitness decline in mitochondrial (mt)DNA-encoded genes. Bilaterian mitochondria-encoded tRNA genes, key players in mitochondrial activity, have accumulated mutations at significantly higher rates than their cytoplasmic counterparts, resulting in foreshortened and fragile structures. Here we show that fragility of mt tRNAs coincided with the evolution of bilaterian animals. We demonstrate that bilaterians compensated for this reduced structural complexity in mt tRNAs by sequence-independent induced-fit adaption to the cognate mitochondrial aminoacyl-tRNA synthetase (aaRS). Structural readout by nuclear-encoded aaRS partners relaxed the sequence constraints on mt tRNAs and facilitated accommodation of functionally disruptive mutational insults by cis-acting epistatic compensations. Our results thus suggest that mutational freedom in mt tRNA genes is an adaptation to increased mutation pressure that was associated with the evolution of animal complexity.

Suggested Citation

  • Bernhard Kuhle & Joseph Chihade & Paul Schimmel, 2020. "Relaxed sequence constraints favor mutational freedom in idiosyncratic metazoan mitochondrial tRNAs," Nature Communications, Nature, vol. 11(1), pages 1-12, December.
    • Handle: RePEc:nat:natcom:v:11:y:2020:i:1:d:10.1038_s41467-020-14725-y
    DOI: 10.1038/s41467-020-14725-y
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    Cited by:

    1. Bernhard Kuhle & Marscha Hirschi & Lili K. Doerfel & Gabriel C. Lander & Paul Schimmel, 2022. "Structural basis for shape-selective recognition and aminoacylation of a D-armless human mitochondrial tRNA," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    2. Bernhard Kuhle & Marscha Hirschi & Lili K. Doerfel & Gabriel C. Lander & Paul Schimmel, 2023. "Structural basis for a degenerate tRNA identity code and the evolution of bimodal specificity in human mitochondrial tRNA recognition," Nature Communications, Nature, vol. 14(1), pages 1-13, December.

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